The Ecology of Phytoplankton

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Phytoplankton communities dominate the pelagic Board and as a tutor with the Field Studies Coun- ecosystems that cover 70% of the world’s surface cil. In 1970, he joined the staff at the Windermere area. In this marvellous new book Colin Reynolds Laboratory of the Freshwater Biological Association. deals with the adaptations, physiology and popula- He studied the phytoplankton of eutrophic meres, tion dynamics of the phytoplankton communities then on the renowned ‘Lund Tubes’, the large lim- of lakes and rivers, of seas and the great oceans. netic enclosures in Blelham Tarn, before turning his The book will serve both as a text and a major attention to the phytoplankton of rivers. During the work of reference, providing basic information on 1990s, working with Dr Tony Irish and, later, also Dr composition, morphology and physiology of the Alex Elliott, he helped to develop a family of models main phyletic groups represented in marine and based on, the dynamic responses of phytoplankton freshwater systems. In addition Reynolds reviews populations that are now widely used by managers. recent advances in community ecology, developing He has published two books, edited a dozen others an appreciation of assembly processes, coexistence and has published over 220 scientiﬁc papers as and competition, disturbance and diversity. Aimed well as about 150 reports for clients. He has primarily at students of the plankton, it develops given advanced courses in UK, Germany, Argentina, many concepts relevant to ecology in the widest Australia and Uruguay. He was the winner of the sense, and as such will appeal to a wide readership 1994 Limnetic Ecology Prize; he was awarded a cov- among students of ecology, limnology and oceanog- eted Naumann–Thienemann Medal of SIL and was raphy. honoured by Her Majesty the Queen as a Member of Born in London, Colin completed his formal edu- the British Empire. Colin also served on his munici- cation at Sir John Cass College, University of Lon- pal authority for 18 years and was elected mayor of don. He worked brieﬂy with the Metropolitan Water Kendal in 1992–93. ecology, biodiversity, and conservation

Series editors Michael Usher University of Stirling, and formerly Scottish Natural Heritage Denis Saunders Formerly CSIRO Division of Sustainable Ecosystems, Canberra Robert Peet University of North Carolina, Chapel Hill Andrew Dobson Princeton University

Editorial Board Paul Adam University of New South Wales, Australia H. J. B. Birks University of Bergen, Norway Lena Gustafsson Swedish University of Agricultural Science Jeff McNeely International Union for the Conservation of Nature R. T. Paine University of Washington David Richardson University of Cape Town Jeremy Wilson Royal Society for the Protection of Birds

The world’s biological diversity faces unprecedented threats. The urgent challenge facing the concerned biologist is to understand ecological processes well enough to maintain their functioning in theface of the pressures resulting from human population growth. Those concerned with the conservation of biodiversity and with restoration also need to be acquainted with the political, social, historical, economic and legal frameworks within which ecological and conservation practice must be developed. This series will present balanced, comprehensive, up-to-date and critical reviews of selected topics within the sciences of ecology and conservation biology, both botanical and zoological, and both ‘pure’ and ‘applied’. It is aimed at advanced (ﬁnal-year undergraduates, graduate students, researchers and university teachers, as well as ecologists and conservationists in industry, government and the voluntary sectors. The series encompasses a wide range of approaches and scales (spatial, temporal, and taxonomic), including quantitative, theoretical, population, community, ecosystem, landscape, historical, experimental, behavioural and evolutionary studies. The emphasis is on science related to the real world of plants and animals, rather than on purely theoretical abstractions and mathematical models. Books in this series will, wherever possible, consider issues from a broad perspective. Some books will challenge existing paradigms and present new ecological concepts, empirical or theoretical models, and testable hypotheses. Other books will explore new approaches and present syntheses on topics of ecological importance. Ecology and Control of Introduced Plants Judith H. Myers and Dawn R. Bazely Invertebrate Conservation and Agricultural Ecosystems T. R. New Risks and Decisions for Conservation and Environmental Management Mark Burgman Nonequilibrium Ecology Klaus Rohde Ecology of Populations Esa Ranta, Veijo Kaitala and Per Lundberg The Ecology of Phytoplankton

C. S. Reynolds cambridge university press Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo

Cambridge University Press The Edinburgh Building, Cambridge cb2 2ru,UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Informationonthistitle:www.cambridge.org/9780521844130

This publication is in copyright. Subject to statutory exception and to the provision of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press.

First published in print format 2006 isbn-13 978-0-511-19094-0 eBook (EBL) isbn-10 0-511-19094-8 eBook (EBL) isbn-13 978-0-521-84413-0 hardback isbn-10 0-521-84413-4 hardback isbn-13 978-0-521-60519-9 paperback isbn-10 0-521-60519-9 paperback

Cambridge University Press has no responsibility for the persistence or accuracy of urls for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. This book is dedicated to my wife, JEAN, to whom its writing represented an intrusion into domestic life, and to Charles Sinker, John Lund and Ramon´ Margalef. Each is a constant source of inspiration to me.

Contents

Preface page ix Acknowledgements xii

Chapter 1. Phytoplankton1 1.1 Deﬁnitions and terminology 1 1.2 Historical context of phytoplankton studies 3 1.3The diversiﬁcation of phytoplankton 4 1.4General features of phytoplankton 15 1.5Theconstructionandcompositionoffreshwater phytoplankton 24 1.6 Marine phytoplankton 34 1.7 Summary 36

Chapter 2. Entrainment and distribution in the pelagic 38 2.1 Introduction 38 2.2 Motion in aquatic environments 39 2.3 Turbulence 42 2.4 Phytoplankton sinking and ﬂoating 49 2.5 Adaptive and evolutionary mechanisms for

regulating ws 53 2.6 Sinking and entrainment in natural turbulence 67 2.7 The spatial distribution of phytoplankton 77 2.8 Summary 90

Chapter 3. Photosynthesis and carbon acquisition in phytoplankton 93 3.1 Introduction 93 3.2 Essential biochemistry of photosynthesis 94 3.3 Light-dependent environmental sensitivity of photosynthesis 101 3.4 Sensitivity of aquatic photosynthesis to carbon sources 124 3.5 Capacity, achievement and fate of primary production at the ecosystem scale 131 3.6 Summary 143

Chapter 4. Nutrient uptake and assimilation in phytoplankton 145 4.1 Introduction 145 4.2 Cell uptake and intracellular transport of nutrients 146 4.3 Phosphorus: requirements, uptake, deployment in phytoplankton 151 viii CONTENTS

4.4 Nitrogen: requirements, sources, uptake and metabolism in phytoplankton 161 4.5 The role of micronutrients 166 4.6 Major ions 171 4.7 Silicon: requirements, uptake, deployment in phytoplankton 173 4.8 Summary 175

Chapter 5. Growth and replication of phytoplankton 178 5.1 Introduction: characterising growth 178 5.2 The mechanics and control of growth 179 5.3 The dynamics of phytoplankton growth and replication in controlled conditions 183 5.4 Replication rates under sub-ideal conditions 189 5.5 Growth of phytoplankton in natural environments 217 5.6 Summary 236

Chapter 6. Mortality and loss processes in phytoplankton 239 6.1 Introduction 239 6.2 Wash-out and dilution 240 6.3 Sedimentation 243 6.4 Consumption by herbivores 250 6.5 Susceptibility to pathogens and parasites 292 6.6 Death and decomposition 296 6.7 Aggregated impacts of loss processes on phytoplankton composition 297 6.8 Summary 300

Chapter 7. Community assembly in the plankton: pattern, process and dynamics 302 7.1Introduction 302 7.2 Patterns of species composition and temporal change in phytoplankton assemblages 302 7.3 Assembly processes in the phytoplankton 350 7.4 Summary 385

Chapter 8. Phytoplankton ecology and aquatic ecosystems: mechanisms and management 387 8.1 Introduction 387 8.2 Material transfers and energy ﬂow in pelagic systems 387 8.3 Anthropogenic change in pelagic environments 395 8.4 Summary 432 8.5 A last word 435

Glossary 437 Units, symbols and abbreviations 440 CONTENTS ix

References 447 Index to lakes, rivers and seas 508 Index to genera and species of phytoplankton 511 Index to genera and species of other organisms 520 General index 524

Preface

This is the third book I have written on the sub- thepresent volume to address more overtly the ject of phytoplankton ecology. When I finished marine phytoplankton, I have set out to construct the first, The Ecology of Freshwater Phytoplankton anew perspective on the expanded knowledge (Reynolds, 1984a), I vowed that it would also be base. I have to say at once that the omission of my last. I felt better about it once it was pub- ‘freshwater’ from the new title does not imply lished but, as I recognised that science was mov- that the book covers the ecology of marine plank- ing on, I became increasingly frustrated about ton in equivalent detail. It does, however, signify the growing datedness of its information. When agenuine attempt to bridge the deep but wholly an opportunity was presented to me, in the form artificial chasm that exists between marine and of the 1994 Ecology Institute Prize, to write my freshwater science, which political organisation second book on the ecology of plankton, Vege- and science funding have perpetuated. tation Processes in the Pelagic (Reynolds, 1997a), I Atapersonal level, this wider view is a satisfy- was abletodrawontheenormous strides that ing thing to develop, being almost a plea for abso- were being made towards understanding the part lution – ‘I am sorry for getting it wrong before, played by the biochemistry, physiology and pop- this is what I should have said!’ At a wider level, I ulation dynamics of plankton in the overall func- am conscious that many people still use and fre- tioning of the great aquatic ecosystems. Any feel- quently cite my 1984 book; I would like them to ing of satisfaction that that exercise brought to know that I no longer believe everything, or even me has also been overtaken by events of the last very much, of what I wrote then. As if to empha- decade, which have seen new tools deployed to sise this, I have adopted a very similar approach thegreater amplification of knowledge and new to thesubject, again using eight chapters (albeit facts uncovered to be threaded into the web of with altered titles). These are developed accord- understanding of how the world works. ing to a similar sequence of topics, through mor- Of course, this is the way of science. There phology, suspension, ecophysiology and dynam- is no scientific text that can be closed with a ics to the structuring of communities and their sigh, ‘So that’s it, then’. There are always more functions within ecosystems. This arrangement questions. I actually have rather more now than allows me to contrast directly the new knowl- I had at the same stage of finishing the 1984 vol- edge and the understanding it has rendered ume. No, the best that can be expected, or even redundant. hoped for, is a periodic stocktake: ‘This is what So just what are these mould-breaking we have learned, this is how we think we can findings? In truth, they impinge upon the sub- explain things and this is where it fits into what ject matter in each of the chapters. Advances in we thought we knew already; this will stand until microscopy have allowed ultrastructural details we learn something else.’ This is truly the way of planktic organisms to be revealed for the first of science. Taking observations, verifying them time. The advances in molecular biology, in par- by experimentation, moving from hypothesis to ticular the introduction of techniques for iso- fact, we are able to formulate progressively closer lating chromosomes and ribosomes, fragmenting approximations to the truth. them by restriction enzymes and reading genetic In fact, the second violation of my 1984 vow sequences, have totally altered perceptions about has a more powerful and less high-principled phyletic relationships among planktic taxa and driver. Itisjustthattheprogressinplankton suppositions about their evolution. The classifica- ecology since 1984 has been astounding, turning tion of organisms is undergoing change of revolu- almost each one of the first book’s basic assump- tionary proportions, while morphological variations on its head. Besides widening the scope of tion among (supposedly) homogeneous genotypes xii PREFACE

questions the very concept of putting names phytoplankton photosynthesis that is leaked or to individual organisms. At the scale of cells, actively discharged into the water. Far from hold- the whole concept of how they are moved in ing to the traditional view of the pelagic food thewater has been addressed mathematically. chain – algae, zooplankton, fish – plankton ecol- It is now appreciated that planktic cells experi- ogists now have to acknowledge that marine ence critical physical forces that are very differ- food webs are regulated ‘by a sea of microbes’ ent from those affecting (say) fish: viscosity and (Karl, 1999), through the muliple interactions of small-scale turbulence determine the immediate organic and inorganic resources and by the lock environment of microorganisms; surface tension of protistan predators and acellular pathogens is a lethal and inescapable spectre; while shear (Smetacek, 2002). Even in lakes, where the case forces dominate dispersion and the spatial dis- for the top–down control of phytoplankton by tributions of populations. These discoveries flow herbivorous grazers is championed, the other- from the giant leaps in quantification and mea- wise dominant microbially mediated supply of surements made by physical limnologists and resources to higher trophic levels is demonstra- oceanographers since the early 1980s. These have bly subsidised by components from the littoral also impinged on the revision of how sinking (Schindler et al., 1996;Vadeboncoeur et al., 2002). and settlement of phytoplankton are viewed and There have been many other revolutions. One they have helped to consolidate a robust theory more to mention here is the progress in ecosys- of filter-feeding by zooplankton. tem ecology, or more particularly, the bridge The way in which nutrients are sequestered between the organismic and population ecology from dilute and dispersed sources in the water and the behaviour of entire systems. How ecosys- and then deployed in the assembly and replica- tems behave, how their structure is maintained tion of new generations of phytoplankton has and what is critical to that maintenance, what been intensively investigated by physiologists. thebiogeochemical consequences might be and Recent findings have greatly modified percep- how they respond to human exploitation and tions about what is meant by ‘limiting nutrients’ management, have all become quantifiable. The and what happens when one or other is in short linking threads are based upon thermodynamic supply. As Sommer (1996) commented, past sup- rules of energy capture, exergy storage and struc- positions about the repercussions on community tural emergence, applied through to the systems structure have had to be revised, both through level (Link, 2002; Odum, 2002). thedirect implications for interspecific compe- In the later chapters in this volume, I attempt tition for resources and, indirectly, through the to apply these concepts to phytoplankton-based effects of variable nutritional value of potential systems, where the opportunity is again taken foods to the web of dependent consumers. to emphasise the value to the science of ecol- Arguably, the greatest shift in understanding ogy of studying the dynamics of microorganisms concerns the way in which the pelagic ecosys- in the pursuit of high-order pattern and assem- temworks. Although the abundance of plank- bly rules (Reynolds, 1997, 2002b). The dual chal- tic bacteria and the relatively vast reserve of lenge remains, to convince students of forests dissolved organic carbon (DOC) had long been and other terrestrial ecosystems that microbial recognised, the microorganismic turnover of car- systems do conform to analogous rules, albeit bon has only been investigated intensively dur- at very truncated real-time scales, and to per- ing the last two decades. It was soon recog- suade microbiologists to look up from the micro- nised that the metazoan food web of the open scope for long enough to see how their knowl- oceans is linked to the producer network via edge might be applied to ecological issues. the turnover of the microbes and that this state- Iamproud to acknowledge the many people ment applies to many larger freshwater systems who have influenced or contributed to the sub- as well. The metabolism of the variety of subject matter of this book. I thank Charles Sinker stances embraced by ‘DOC’ varies with source and forinspiring a deep appreciation of ecology and chain length but a labile fraction originates from its mechanisms. I am grateful to John Lund, CBE, PREFACE xiii

FRS for the opportunity to work on phytoplank- among whom special thanks are due to Tony tonasapostgraduate and for the constant inspi- Irish, Sheila Wiseman, George Jaworski and Brian ration and access to his knowledge that he has Godfrey. Peter Allen, Christine Butterwick, Julie given me. Of the many practising theoretical ecol- Corry (later Parker), Mitzi De Ville, Joy Elsworth, ogists whose works I have read, I have felt the Alastair Ferguson, Mark Glaister, David Gouldney, greatest affinity to the ideas and logic of Ramon´ Matthew Rogers, Stephen Thackeray and Julie Margalef; I greatly enjoyed the opportunities to Thompson also worked with me at particular discuss these with him and regret that there will times. Throughout this period, I was privileged be no more of them. to work in a ‘well-found’ laboratory with abun- Igratefully acknowledge the various scien- dant technical and practical support. I freely tists whose work has profoundly influenced par- acknowledge use of the world’s finest collection ticular parts of this book and my thinking gen- of the freshwater literature and the assistance erally. They include (in alphabetical order) Sal- provided at various times by John Horne, Ian lie Chisholm, Paul Falkowski, Maciej Gliwicz, Pettman, Ian McCullough, Olive Jolly and Mari- Phil Grime, Alan Hildrew, G. E. Hutchinson, Jorg¨ lyn Moore. Secretarial assistance has come from Imberger, Petur Jonasson,´ Sven-Erik Jørgensen, Margaret Thompson, Elisabeth Evans and Joyce Dave Karl, Winfried Lampert, John Lawton, John Hawksworth. Trevor Furnass has provided abun- Raven, Marten Scheffer, Ted Smayda, Milan dant reprographic assistance over many years. I Straˇskraba, Reinhold Tuxen,¨ Anthony Walsby and am forever in the debt of Hilda Canter-Lund, FRPS Thomas Weisse. I have also been most fortu- forthe use of her internationally renowned pho- nate in having been able, at various times, to tomicrographs. work with and discuss many ideas with col- Aspecial word is due to the doctoral students leagues who include Keith Beven, Sylvia Bonilla, whom I have supervised. The thirst for knowl- Odécio Caceres,´ Paul Carling, Jean-Pierre Descy, edge and understanding of a good pupil gener- Monica´ Diaz, Graham Harris, Vera Huszar, Dieter ally provide a foil and focus in the other direc- Imboden, Kana Ishikawa, Medina Kadiri, Susan tion. I owe much to the diligent curiosity of Chris Kilham, Michio Kumagai, Bill Li, Vivian Monte- van Vlymen, Helena Cmiech, Karen Saxby (now cino, Mohi Munawar, Masami Nakanishi, Shin- Rouen), Sianˆ Davies, Alex Elliott, Carla Kruk and Ichi Nakano, Luigi Naselli-Flores, Pat Neale, Søren Phil Davis. Nielsen, Judit Padisak,´ Fernando Pedrozo, Victor My final word of appreciation is reserved for Smetaˇcek, Ulrich Sommer, José Tundisi and acknowledgement of the tolerance and forbear- Peter Tyler. I am especially grateful to Cather- ance of my wife and family. I cheered through ine Legrand who generously allowed me to use many juvenile football matches and dutifully and interpret her experimental data on Alexan- attended a host of ballet and choir performances drium.Nearer to home, I have similarly benefited and, yes, it was quite fun to relive three more from long and helpful discussions with such erst- school curricula. Nevertheless, my children had while Windermere colleagues as Hilda Canter- less of my time than they were entitled to expect. Lund, Bill Davison, Malcolm Elliott, Bland Finlay, Jean has generously shared with my science the Glen George, Ivan Heaney, Stephen Maberly, Jack full focus of my attention. Yet, in 35 years of mar- Talling and Ed Tipping. riage, she has never once complained, nor done During my years at The Ferry House, I was less than encourage the pursuit of my work. I am ably and closely supported by several co-workers, proud to dedicate this book to her. Acknowledgements

Except where stated, the illustrations in this book the copyright of Blackwell Science (the specific are reproduced, redrawn or otherwise slightly sources are noted in the figure captions) and are modified from sources noted in the individual redrawn by permission. captions. The author and the publisher are grate- Figures 3.7, 3.15, 4.6 and 7.2.3 (or parts thereof) ful to the various copyright holders, listed below, are redrawn from Freshwater Biology by permission who have given permission to use copyright mate- of Blackwell Science. rial in this volume. While every effort has been made to clear permissions as appropriate, the Figure 3.7 incorporates items redrawn from Bio- publisher would appreciate notification of any logical Reviews with acknowledgement to the Cam- omission. bridge Philosophical Society. Figures 1.1 to 1.8, 1.10, 2.8 to 2.13, 2.17, 2.20 to Figure 5.9 is redrawn by permission of John Wiley 2.31, 3.3 to 3.9, 3.16 and 3.17, 5.20, 6.2, 6.7, 6.11. & Sons Ltd. 7.6 and 7.18 are already copyrighted to Cambridge University Press. Figure 5.14 is redrawn by permission of Springer- Verlag GmbH. Figure 1.9 is redrawn by permission of Oxford University Press. Figures 5.15 to 5.17, 5.19, 6.8 and 6.9 are redrawn by permission of SpringerScience+Business BV. Figure 1.11 is the copyright of the American Soci- ety of Limnology and Oceanography. Figures 6.12, 6.15, 7.1 to 7.4, 7.9 and 8.6 are reproduced from Journal of Plankton Research by permis- Figures 2.1 and 2.2, 2.5 to 2.7, 2.15 and 2.16, 2.18 sion of Oxford University Press. Dr K. Bruning also and 2.19, 3.12, 3.14, 3.19, 4.1, 4.3 to 4.5, 5.1 to gave permission to produce Fig. 6.12. 5.5, 5.8, 5.10, 5.12 and 5.13, 5.20 and 5.21, 6.1, 6.2, 6.4, 6.14, 7.8, 7.10 and 7.11, 7.14, 7.16 and 7.17, Figure 7.7 is redrawn by permission of the Direc- 7.20 and 7.22 are redrawn by permission of The tor, Marine Biological Association. Ecology Institute, Oldendorf. Figures 7.12 to 7.14, 7.24 and 7.25 are redrawn Figures 2.3 and 4.7 are redrawn from the source from Verhandlungen der internationale Vereini- noted in the captions, with acknowledgement to gung fur¨ theoretische und angewandte Limnolo- Artemis Press. gie by permission of Dr E. Nagele¨ (Publisher) (http://www.schwezerbart.de). Figures 2.4, 3.18, 5.11, 5.18, 7.5, 7.15, 8.2 and 8.3 are redrawn from the various sources noted in Figure 7.19 is redrawn with acknowledgement to the respective captions and with acknowledge- theAthlone Press of the University of London. ment to Elsevier Science, B.V. Figure 7.21 is redrawn from Aquatic Ecosystems Figure 2.14 is redrawn from the British Phycologi- Health and Management by permission of Taylor cal Journal by permission of Taylor & Francis Ltd &Francis, Inc. (http://www.taylorandfrancis.com). (http://www.tandf.co.uk/journals). Figure 8.1 is redrawn from Scientia Maritima by Figure 3.1 is redrawn by permission of Nature permission of Institut de Ciències del Mar. Publishing Group. Figures 8.5, 8.7 and 8.8 are redrawn by permis- Figures 3.2, 3.11, 3.13, 4.2, 5.6, 6.4, 6.6, 6.9, sion of the Chief Executive, Freshwater Biological 6.10 and 6.13 come from various titles that are Association. Chapter 1

Phytoplankton

and are not necessarily contested. Thus, ‘plank- 1.1 Definitions and terminology ton’ excludes other suspensoids that are either non-living, such as clay particles and precipitated The correct place to begin any exposition of a chemicals, or are fragments or cadavers derived major component in biospheric functioning is from biogenic sources. Despite the existence of with precise definitions and crisp discrimination. thenow largely redundant subdivision tychoplank- This should be a relatively simple exercise but for ton (see Box 1.1), ‘plankton’ normally comprises the need tosatisfy a consensus of understand- those living organisms that are only fortuitously ing and usage. Particularly among the biological and temporarily present, imported from adjacent sciences, scientific knowledge is evolving rapidly habitats but which neither grew in this habitat and, as it does so, it often modifies and outgrows nor are suitably adapted to survive in the truly the constraints of the previously acceptable ter- open water, ostensibly independent of shore and minology. I recognised this problem for plank- bottom. Such locations support distinct suites of ton science in an earlier monograph (Reynolds, surface-adhering organisms with their own dis- 1984a). Since then, the difficulty has worsened tinctive survival adaptations. and it impinges on many sections of the present ‘Suspension’ has been more problematic, hav- book. The best means of dealing with it is to ing quite rigid physical qualifications of dens- accept the issue as a symptom of the good health ity and movement relative to water. As will be and dynamism of the science and to avoid con- rehearsed in Chapter 2, only rarely can plank- straining future philosophical development by a ton be isopycnic (having the same density) with redundant terminological framework. themedium and will have a tendency to float The need for definitions is not subverted, how- upwards or sink downwards relative to it. The ever, but it transforms to an insistence that those rate of movement isalsosizedependent,so that are ventured are provisional and, thus, open that ‘apparent suspension’ is most consistently to challenge and change. Tobeabletoreveal achieved by organisms of small (<1mm)size. something also of the historical context of the Crucially, this feature is mirrored in the fact usage is to give some indication of the limitations that the intrinsic movements of small organisms of the terminology and of the areas of conjecture are frequently too feeble to overcome the veloc- impinging upon it. ity and direction of much of the spectrum of So it is with ‘plankton’. The general under- watermovements. The inability to control hori- standing of this term is that it refers to the col- zontal position or to swim against significant cur- lective of organisms that are adapted to spend part rents in open waters separates ‘plankton’ from or all of their lives in apparent suspension in the the‘nekton’ of active swimmers, which include open water of the sea, of lakes, ponds and rivers. adult fish, large cephalopods, aquatic reptiles, The italicised words are crucial to the concept birds and mammals. 2 PHYTOPLANKTON

Box 1.1 Some deﬁnitions used in the literaure on plankton

seston the totality of particulate matter in water; all material not in solution tripton non-living seston plankton living seston, adapted for a life spent wholly or partly in quasi-suspension in open water, and whose powers of motility do not exceed turbulent entrainment (see Chapter 2) nekton animals adapted to living all or part of their lives in open water but whose intrinsic movements are almost independent of turbulence euplankton redundant term to distinguish fully adapted, truly planktic organisms from other living organisms fortuitously present in the water tychoplankton non-adapted organisms from adjacent habitats and present in the water mainly by chance meroplankton planktic organisms passing a major part of the life history out of the plankton (e.g. on the bottom sediments) limnoplankton plankton of lakes heleoplankton plankton of ponds potamoplankton plankton of rivers phytoplankton planktic photoautotrophs and major producer of the pelagic bacterioplankton planktic prokaryotes mycoplankton planktic fungi zooplankton planktic metazoa and heterotrophic protistans

Some more, now redundant, terms The terms nannoplankton, ultraplankton, µ-algae are older names for various smaller size categories of phytoplankton, eclipsed by the classiﬁcation of Sieburth et al. (1978) (see Box 1.2).

In this way, plankton comprises organisms isms, their phyletic affinities and physiological that range in size from that of viruses (a few tens capabilities has expanded, it has become clear of nanometres) to those of large jellyfish (a metre that the divisions used hitherto do not pre- or more). Representative organisms include bac- cisely coincide: there are photosynthetic bacteria, protistans, fungi and metazoans. In the teria, phagotrophic algae and flagellates that take past, it has seemed relatively straightforward to up organic carbon from solution. Here, as in gen- separate the organisms of the plankton, both eral, precision will be considered relevant and into broad phyletic categories (e.g. bacterioplank- important in the context of organismic prop- ton, mycoplankton) or into similarly broad func- erties (their names, phylogenies, their morpho- tional categories (photosynthetic algae of the logical and physiological characteristics). On the phytoplankton, phagotrophic animals of the zoo- other hand, the generic contributions to sys- plankton). Again, as knowledge of the organ- tems (at the habitat or ecosystem scales) of the HISTORICAL CONTEXT OF PHYTOPLANKTON STUDIES 3 photosynthetic primary producers, phagotrophic tion to English is ‘up drive’, approximately ‘buoy- consumers and heterotrophic decomposers may ancy’ or ‘flotation’, a clear reference to Muller’s¨ be attributed reasonably but imprecisely to phyto- assumption that the material floated up to the plankton, zooplankton and bacterioplankton. surface waters – like so much oceanic dirt! It The defintion of phytoplankton adopted for took one of Muller’s¨ students, Ernst Haeckel, to this book is the collective of photosynthetic champion the beauty of planktic protistans and microorganisms, adapted to live partly or contin- metazoans. His monograph on the Radiolaria uously in open water. As such, it is the photoau- was also one of the first to embrace Darwin’s totrophic part of the plankton and a major pri- (1859)evolutionary theory in order to show mary producer of organic carbon in the pelagic structural affinities and divergences. Haeckel, of of the seas and of inland waters. The distinction course, became best known for his work on of phytoplankton from other categories of plank- morphology, ontogeny and phylogeny. According ton and suspended matter are listed in Box 1.1. to Smetacek et al.(2002), his interest and skills It may be added that it is correct to refer to as a draughtsman advanced scientific awareness phytoplankton as a singular term (‘phytoplank- of the range of planktic form (most significantly, ton is’ rather than ‘phytoplankton are’). A single Haeckel, 1904) but to the detriment of any real organism is a phytoplanktont or (more ususally) progress in understanding of functional differen- phytoplankter.Incidentally, the adjective ‘plank- tiation. Until the late 1880s, it was not appreci- tic’ is etymologically preferable to the more com- ated that the organisms of the Auftrieb,eventhe monly used ‘planktonic’. algae among them, could contribute much to the nutrition of the larger animals of the sea. Instead, it seems to have been supposed that organic mat- 1.2 Historical context of terinthe fluvial discharge from the land was the major nutritive input. It is thus rather interest- phytoplankton studies ing to note that, a century or so later, this possibility has enjoyed something of a revival (see The first use of the term ‘plankton’ is attributed Chapters 3 and 8). in several texts (Ruttner, 1953;Hutchinson, 1967) If Haeckel had conveyed the beauty of the to Viktor Hensen, who, in the latter half of the pelagic protistans, it was certainly Viktor Hensen nineteenth century, began to apply quantitative who had been more concerned about their role methods to gauge the distribution, abundance in a functional ecosystem. Hensen was a phys- and productivity of the microscopic organisms iologist who brought a degree of empiricism of the open sea. The monograph that is usually to his study of the perplexing fluctuations in cited (Hensen, 1887)is, in fact, rather obscure NorthSea fish stocks. He had reasoned that and probably not well read in recent times but fish stocks and yields were related to the pro- Smetacek et al.(2002)haveprovidedaprobing duction and distribution of the juvenile stages. and engaging review of the original, within the Through devising techniques for sampling, quan- context of early development of plankton science. tification and assessing distribution patterns, Most of the present section is based on their always carefully verified by microscopic exami- article. nation, Hensen recognised both the ubiquity of The existence of a planktic community of phytoplankton and its superior abundance and organisms in open water had been demonstrated quality over coastal inputs of terrestrial detritus. many years previously by Johannes Muller.¨ Knowl- He saw the connection between phytoplankton edge of some of the organisms themselves and the light in the near-surface layer, the nutri- stretches further back, to the earliest days tive resource it provided to copepods and other of microscopy. From the 1840s, Muller¨ would small animals, and the value of these as a food demonstrate net collections to his students, using source to fish. the word Auftrieb to characterise the commu- Thus, in addition to bequeathing a new nity (Smetacek et al., 2002). The literal transla- name for the basal biotic component in pelagic 4 PHYTOPLANKTON

ecosystems, Hensen may be regarded justifiably latter quest occupies most of the rest of the book. as the first quantitative plankton ecologist and However, it is not giving away too much to antici- as the person who established a formal method- pate that systematics provides an important foun- ology for its study. Deducing the relative contri- dation for species-specific physiology and which butions of Hensen and Haeckel to the founda- is itself part-related to morphology. Accordingly, tion of modern plankton science, Smetacek et al. great attention is paid here to the differentia- (2002) concluded that it is the work of the lat- tion of individualistic properties of representa- ter that has been the more influential. This is an tive species of phytoplankton. opinion with which not everyone will agree but However, there is value in being able simul- this is of little consequence. However, Smetacek taneously to distinguish among functional cate- et al.(2002)offeredamostprofoundandresonant gories (trees from herbs!). The scaling system and observation in suggesting that Hensen’s general nomenclature proposed by Sieburth et al.(1978) understanding of the role of plankton (‘the big has been widely adopted in phytoplankton ecol- picture’) was essentially correct but erroneous in ogy to distinguish functional separations within its details, whereas in Haeckel’s case, it was the the phytoplankton. It has also eclipsed the use of other way round. Nevertheless, both have good such terms as µ-algae and ultraplankton to separate claim to fatherhood of plankton science! thelower size range of planktic organisms from those (netplankton)large enough to be retained by themeshes of a standard phytoplankton net. 1.3 The diversification of The scheme of prefixes has been applied to size categories of zooplankton, with equal success. phytoplankton The size-based categories are set out in Box 1.2. At thelevel of phyla, the classification of Current estimates suggest that between 4000 and thephytoplankton is based on long-standing cri- 5000 legitimate species of marine phytoplank- teria, distinguished by microscopists and bio- tonhavebeen described (Sournia et al. 1991; chemists over the last 150 years or so, from Tett and Barton, 1995). I have not seen a com- which there is little dissent. In contrast, subdi- parable estimate for the number of species in vision within classes, orders etc., and the tracing inland waters, beyond the extrapolation I made of intraphyletic relationships, affinities within (Reynolds, 1996a)thatthenumberisunlikelyto and among families, even the validity of suppos- be substantially smaller. In both lists, there is edly well-characterised species, has become sub- not just a large number of mutually distinct taxa ject to massive reappraisal. The new factor that of photosynthetic microorganisms but there is a has come into play is the powerful armoury of wide variety of shape, size and phylogenetic affin- themolecular biologists, including the methods ity. As has also been pointed out before (Reynolds, forreading gene sequences and for the statisti- 1994a), the morphological range is comparable to cal matching of these to measure the closeness the one spanning forest trees and the herbs that to other species. grow at their base. The phyletic divergence of the Of course, the potential outcome is a much representatives is yet wider. It would be surpris- more robust, genetically verified family tree of ing if the species of the phytoplankton were uni- authentic species of phytoplankton. This may be form in their requirements, dynamics and sus- some years away. For the present, it seems point- ceptibilities to loss processes. Once again, there less to reproduce a detailed classification of the is a strong case for attempting to categorise the phytoplankton that will soon be made redun- phytoplankton both on the phylogeny of organ- dant. Even the evolutionary connectivities among isms and on the functional basis of their roles in thephyla and their relationship to the geochem- aquatic ecosystems. Both objectives are adopted ical development of the planetary structures for the writing of this volume. Whereas the for- are undergoing deep re-evaluation (Delwiche, mer is addressed only in the present chapter, the 2000;Falkowski, 2002). For these reasons, the THE DIVERSIFICATION OF PHYTOPLANKTON 5

Box 1.2 The classiﬁcation of phytoplankton according to the scaling nomenclature of Sieburth et al. (1978)

Maximum linear dimension Namea 0.2–2 µm picophytoplankton 2–20 µm nanophytoplankton 20–200 µm microphytoplankton 200 µm–2 mm mesophytoplankton >2mm macrophytoplankton

aThe preﬁxes denote the same size categories when used with ‘-zooplankton’, ‘-algae’, ‘-cyanobacteria’, ‘ﬂagellates’, etc.

taxonomic listings in Table 1.1 are deliberately modern plants, water is the source of reductant conservative. electrons and oxygen is liberated as a by-product Although the life forms of the plankton (oxygenic photosynthesis). Despite their phyletic include acellular microorganisms (viruses) and a proximity to the photoheterotrophs and shar- range of well-characterised Archaea (the halobac- ing a similar complement of bacteriochloro- teria, methanogens and sulphur-reducing bac- phylls (Béjà et al., 2002), the Anoxyphotobac- teria, formerly comprising the Archaebacteria), teria use alternative sources of electrons and, the mostbasicphotosynthetic organisms of the in consequence, generate oxidation products phytoplankton belong to the Bacteria (formerly, other than oxygen (anoxygenic photosynthesis). Eubacteria). The separation of the ancestral bac- Their modern-day representatives are the purple teria fromthearchaeans (distinguished by the and green sulphur bacteria of anoxic sediments. possession of membranes formed of branched Some of these are planktic in the sense that hydrocarbons and ether linkages, as opposed to they inhabit anoxic, intensively stratified layers thestraight-chain fatty acids and ester linkages deep in small and suitably stable lakes. The trait found in the membranes of all other organisms: might be seen as a legacy of having evolved in a Atlas and Bartha, 1993) occurred early in micro- wholly anoxic world. However, aerobic, anoxy- bial evolution (Woese, 1987;Woeseet al., 1990). genic phototrophic bacteria, containing bac- The appearance of phototrophic forms, dis- terichlorophyll a,havebeenisolatedfromoxic tinguished by their crucial ability to use light marine environments (Shiba et al., 1979); it has energy in order to synthesise adenosine triphos- also become clear that their contribution to the phate (ATP) (see Chapter 3), was also an ancient oceanic carbon cycle is not necessarily insignifi- event that took place some 3000 million years ago cant (Kolber et al., 2001;Goericke, 2002). (3 Ga BP (before present)). Some of these organ- Nevertheless, the oxygenic photosynthesis pio- isms were photoheterotrophs, requiring organic neered by the Cyanobacteria from about 2.8 Ga precursors for the synthesis of their own cells. before present has proved to be a crucial step in Modern forms include green flexibacteria (Chlo- theevolution of life in water and, subsequently, roflexaceae) and purple non-sulphur bacteria on land. Moreover, the composition of the atmos- (Rhodospirillaceae), which contain pigments sim- phere was eventually changed through the biolo- ilar to chlorophyll (bacteriochlorophyll a, b or gical oxidation of water and the simultaneous c). Others were true photoautotrophs, capable removal and burial of carbon in marine sedi- of reducing carbon dioxide as a source of cell ments (Falkowski, 2002). Cyanobacterial photo- carbon (photosynthesis). Light energy is used to synthesis is mediated primarily by chlorophyll strip electrons from a donor substance. In most a,borneon thylakoid membranes. Accessory 6 PHYTOPLANKTON

Ta b l e 1.1 Survey of the organisms in the phytoplankton

Domain: BACTERIA Division: Cyanobacteria (blue-green algae) Unicellular and colonial bacteria, lacking membrane bound plastids. Primary photosynthetic pigment is chlorophyll a, with accessory phycobilins (phycocyanin, phycoerythrin). Assimilation products, glycogen, cyanophycin. Four main sub-groups, of which three have planktic representatives. Order: CHROOCOCCALES Unicellular or coenobial Cyanobacteria but never filamentous. Most planktic genera form mucilaginous colonies, and these are mainly in fresh water. Picophytoplanktic formsabundant in the oceans. Includes: Aphanocapsa, Aphanothece, Chroococcus, Cyanodictyon, Gomphosphaeria, Merismopedia, Microcystis, Snowella, Synechococcus, Synechocystis, Woronichinia Order: OSCILLATORIALES Uniseriate–filamentous Cyanobacteria whose cells all undergo division in the same plane. Marine and freshwater genera. Includes: Arthrospira, Limnothrix, Lyngbya, Planktothrix, Pseudanabaena, Spirulina, Trichodesmium, Tychonema Order: NOSTOCALES Unbranched–filamentous Cyanobacteria whose cells all undergo division in the same plane and certain of which may be facultatively differentiated into heterocysts. In the plankton of fresh waters and dilute seas. Includes: Anabaena, Anabaenopsis, Aphanizomenon, Cylindrospermopsis, Gloeotrichia, Nodularia Exempt Division: Prochlorobacteria Order: PROCHLORALES Unicellular and colonial bacteria, lacking membrane-bound plastids. Photosynthetic pigments are chlorophyll a and b,but lack phycobilins. Includes: Prochloroccus, Prochloron, Prochlorothrix Division: Anoxyphotobacteria Mostly unicellular bacteria whose (anaerobic) photosynythesis depends upon an electron donor other than water and so do not generate oxygen. Inhabit anaerobic sediments and (where appropriate) water layers where light penetrates sufficiently. Two main groups: Family: Chromatiaceae (purple sulphur bacteria) Cells able to photosynthesise with sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c. Includes: Chromatium, Thiocystis, Thiopedia. Family: Chlorobiaceae (green sulphur bacteria) Cells able to photosynthesise with sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c. Includes: Chlorobium, Clathrocystis, Pelodictyon. Domain: EUCARYA Phylum: Glaucophyta Cyanelle-bearing organisms, with freshwater planktic representatives. Includes: Cyanophora, Glaucocystis. Phylum: Prasinophyta Unicellular, mostly motile green algae with 1–16 laterally or apically placed flagella, cell walls covered with fine scales and plastids containing chlorophyll a and b. Assimilatory products mannitol, starch. (cont.) THE DIVERSIFICATION OF PHYTOPLANKTON 7

Ta b l e 1.1 (cont.)

CLASS: Pedinophyceae Order: PEDINOMONADALES Small cells, with single lateral flagellum. Includes: Pedinomonas CLASS: Prasinophyceae Order: CHLORODENDRALES Flattened, 4-flagellated cells. Includes: Nephroselmis, Scherffelia (freshwater); Mantoniella, Micromonas (marine) Order: PYRAMIMONADALES Cells with 4 or 8 (rarely 16) flagella arising from an anterior depression. Marine and freshwater. Includes: Pyramimonas Order: SCOURFIELDIALES Cells with two, sometimes unequal, flagella. Known from freshwater ponds. Includes: Scourfieldia Phylum: Chlorophyta (green algae) Green-pigmented, unicellular, colonial, filamentous, siphonaceous and thalloid algae. One or more chloroplasts containing chlorophyll a and b. Assimilation product, starch (rarely, lipid). CLASS: Chlorophyceae Several orders of which the following have planktic representatives: Order: TETRASPORALES Non-flagellate cells embedded in mucilaginous or palmelloid colonies, but with motile propagules. Includes: Paulschulzia, Pseudosphaerocystis Order: VOLVOCALES Unicellular or colonial biflagellates, cells with cup-shaped chloroplasts. Includes: Chlamydomonas, Eudorina, Pandorina, Phacotus, Volvox (in fresh waters); Dunaliella, Nannochloris (marine) Order: CHLOROCOCCALES Non-flagellate, unicellular or coenobial (sometimes mucilaginous) algae, with many planktic genera. Includes: Ankistrodesmus, Ankyra, Botryococcus, Chlorella, Coelastrum, Coenochloris, Crucigena, Choricystis, Dictyosphaerium, Elakatothrix, Kirchneriella, Monorophidium, Oocystis, Pediastrum, Scenedesmus, Tetrastrum Order: ULOTRICHALES Unicellular or mostly unbranched filamentous with band-shaped chloroplasts. Includes: Geminella, Koliella, Stichococcus Order: ZYGNEMATALES Unicellular or filamentous green algae, reproducing isogamously by conjugation. Planktic genera are mostly members of the Desmidaceae, mostly unicellular or (rarely) filmentous coenobia with cells more or less constricted into two semi-cells linked by an interconnecting isthmus. Exclusively freshwater genera. Includes: Arthrodesmus, Closterium, Cosmarium, Euastrum, Spondylosium, Staurastrum, Staurodesmus, Xanthidium (cont.) 8 PHYTOPLANKTON

Ta b l e 1.1 (cont.)

Phylum: Euglenophyta Green-pigmented unicellular biflagellates. Plastids numerous and irregular, containing chlorophyll a and b. Reproduction by longitudinal fission. Assimilation product, paramylon, oil. One Class, Euglenophyceae, with two orders. Order: EUTREPTIALES Cells having two emergent flagella, of approximately equal length. Marine and freshwater species. Includes: Eutreptia Order: EUGLENALES Cells having two flagella, one very short, one long and emergent. Includes: Euglena, Lepocinclis, Phacus, Trachelmonas Phylum: Cryptophyta Order: CRYPTOMONADALES Naked, unequally biflagellates with one or two large plastids, containing chlorophyll a and c2 (but not chlorophyll b); accessory phycobiliproteins or other pigments colour cells brown, blue, blue-green or red; assimilatory product, starch. Freshwater and marine species. Includes: Chilomonas, Chroomonas, Cryptomonas, Plagioselmis, Pyrenomonas, Rhodomonas Phylum: Raphidophyta Order: RAPHIDOMONADALES (syn. CHLOROMONADALES) Biflagellate, cellulose-walled cells; two or more plastids containing chlorophyll a; cells yellow-green due to predominant accessory pigment, diatoxanthin; assimilatory product, lipid. Freshwater. Includes: Gonyostomum Phylum: Xanthophyta (yellow-green algae) Unicellular, colonial, filamentous and coenocytic algae. Motile species generally subapically and unequally biflagellated; two or many more discoid plastids per cell containing chlorophyll a. Cells mostly yellow-green due to predominant accessory pigment, diatoxanthin; assimilation product, lipid. Several orders, two with freshwater planktic representatives. Order: MISCHOCOCCALES Rigid-walled, unicellular, sometimes colonial xanthophytes. Includes: Goniochloris, Nephrodiella, Ophiocytium Order: TRIBONEMATALES Simple or branched uniseriate filamentous xanthophytes. Includes: Tribonema Phylum: Eustigmatophyta Coccoid unicellular, flagellated or unequally biflagellated yellow-green algae with masking of chlorophyll a by accessory pigment violaxanthin. Assimilation product, probably lipid. Includes: Chlorobotrys, Monodus Phylum: Chrysophyta (golden algae) Unicellular, colonial and filamentous. often uniflagellate, or unequally biflagellate algae. Contain chlorophyll a, c1 and c2, generally masked by abundant accessory pigment, fucoxanthin, imparting distinctive golden colour to cells. Cells sometimes naked or or enclosed in an urn-shaped lorica, sometimes with siliceous scales. Assimilation products, lipid, leucosin. Much reclassified group, has several classes and orders in the plankton. (cont.) THE DIVERSIFICATION OF PHYTOPLANKTON 9

Ta b l e 1.1 (cont.)

CLASS: Chrysophyceae Order: CHROMULINALES Mostly planktic, unicellular or colony-forming flagellates with one or two unequal flagella, occasionally naked, often in a hyaline lorica or gelatinous envelope. Includes: Chromulina, Chrysococcus, Chrysolykos, Chrysosphaerella, Dinobryon, Kephyrion, Ochromonas, Uroglena Order: HIBBERDIALES Unicellular or colony-forming epiphytic gold algae but some planktic representatives. Includes: Bitrichia CLASS: Dictyochophyceae Order: PEDINELLALES Radially symmetrical, very unequally biflagellate unicells or coenobia. Includes: Pedinella (freshwater); Apedinella, Pelagococcus, Pelagomonas, Pseudopedinella (marine) CLASS: Synurophyceae Order: SYNURALES Unicellular or colony-forming flagellates, bearing distinctive siliceous scales. Includes: Mallomonas, Synura Phylum: Bacillariophyta (diatoms) Unicellular and coenobial yellow-brown, non-motile algae with numerous discoid plastids, containing chlorophyll a, c1 and c2, masked by accessory pigment, fucoxanthin. Cell walls pectinaceous, in two distinct and overlapping halves, and impregnated with cryptocrystalline silica. Assimilatory products, chrysose, lipids. Two large orders, both conspicuously represented in the marine and freshwater phytoplankton. CLASS: Bacillariophyceae Order: BIDDULPHIALES (centric diatoms) Diatoms with cylindrical halves, sometimes well separated by girdle bands. Some species form (pseudo-)filaments by adhesion of cells at their valve ends. Includes: Aulacoseira, Cyclotella, Stephanodiscus, Urosolenia (freshwater); Cerataulina, Chaetoceros, Detonula, Rhizosolenia, Skeletonema, Thalassiosira (marine) Order: BACILLARIALES (pennate diatoms) Diatoms with boat-like halves, no girdle bands. Some species form coenobia by adhesion of cells on their girdle edges. Includes: Asterionella, Diatoma, Fragilaria, Synedra, Tabellaria (freshwater); Achnanthes, Fragilariopsis, Nitzschia (marine) Phylum: Haptophyta CLASS: Haptophyceae Gold or yellow-brown algae, usually unicellular, with two subequal flagella and a coiled haptonema, but with amoeboid, coccoid or palmelloid stages. Pigments, chlorophyll a, c1 and c2, masked by accessory pigment (usually fucoxanthin). Assimilatory product, chrysolaminarin. Cell walls with scales, sometimes more or less calcified. Order: PAVLOVALES Cells with haired flagella and small haptonema. Marine and freshwater species. Includes: Diacronema, Pavlova (cont.) 10 PHYTOPLANKTON

Ta b l e 1.1 (cont.)

Order: PRYMNESIALES Cells with smooth flagella, haptonema usually small. Mainly marine or brackish but some common in freshwater plankton. Includes: Chrysochromulina, Isochrysis, Phaeocystis, Prymnesium Order: COCCOLITHOPHORIDALES Cell suface covered by small, often complex, flat calcified scales (coccoliths). Exclusively marine. Include: Coccolithus, Emiliana, Florisphaera, Gephyrocapsa, Umbellosphaera Phylum: Dinophyta Mostly unicellular, sometimes colonial, algae with two flagella of unequal length and orientation. Complex plastids containing chlorophyll a, c1 and c2, generally masked by accessory pigments. Cell walls firm, or reinforced with polygonal plates. Assimilation products: starch, oil. Conspicuously represented in marine and freshwater plankton. Two classes and (according to some authorities) up to 11 orders. CLASS: Dinophyceae Biflagellates, with one transverse flagellum encircling the cell, the other directed posteriorly. Order: GYMNODINIALES Free-living, free-swimming with flagella located in well-developed transverse and sulcal grooves, without thecal plates. Mostly marine. Includes: Amphidinium, Gymnodinium, Woloszynskia Order: GONYAULACALES Armoured, plated, free-living unicells, the apical plates being asymmetrical. Marine and freshwater. Includes: Ceratium, Lingulodinium Order: PERIDINIALES Armoured, plated, free-living unicells, with symmetrical apical plates. Marine and freshwater. Includes: Glenodinium, Gyrodinium, Peridinium Order: PHYTODINIALES Coccoid dinoflagellates with thick cell walls but lacking thecal plates. Many epiphytic for part of life history. Some in plankton of humic fresh waters. Includes: Hemidinium CLASS: Adinophyceae Order: PROROCENTRALES Naked or cellulose-covered cells comprising two watchglass-shaped halves. Marine and freshwater species. Includes: Exuviella, Prorocentrum

pigments, called phycobilins, are associated with are recognised, three of which (the chroococ- these membranes, where they are carried in calean, the oscillatorialean and the nostocalean; granular phycobilisomes. Life forms among the thestigonematalean line is the exception) have Cyanobacteria have diversified from simple coc- major planktic representatives that have diversi- coids and rods into loose mucilaginous colonies, fied greatly among marine and freshwater sys- called coenobia, into filamentous and to pseu- tems. The most ancient group of the surviv- dotissued forms. Four main evolutionary lines ing groups of photosynthetic organisms is, in THE DIVERSIFICATION OF PHYTOPLANKTON 11 termsofindividuals, the most abundant on the origin of eukaruote plastids (Bhattacharya and planet. Medlin, 1998; Douglas and Raven, 2003). Prag- Links to eukaryotic protists, plants and ani- matically, we may judge this to have been a mals from the Cyanobacteria had been sup- highly successful combination. There may well posed explicitly and sought implicitly. The dis- have been others of which nothing is known, covery of a prokaryote containing chlorophyll a apart from the small group of glaucophytes that and b but lacking phycobilins, thus resembling carry cyanelles rather than plastids. The cyanelles the pigmentation of green plants, seemed to are supposed to be an evolutionary interme- fit the bill (Lewin, 1981). Prochloron,asymbiont diate between cyanobacterial cells and chloro- of salps, is not itself planktic but is recover- plasts (admittedly, much closer to the latter). able in collections of marine plankton. The first Neither cyanelles nor plastids can grow inde- description of Prochlorothrix from the freshwa- pendently of the eukaryote host and they are ter phytoplankton in the Netherlands (Burger- apportioned among daughters when the host cell Wiersma et al., 1989) helped to consolidate the divides. There is no evidence that the handful impression of an evolutionary ‘missing link’ of of genera ascribed to this phylum are closely chlorophyll-a-and-b-containing bacteria. Then related to each other, so it may well be an arti- came another remarkable finding: the most ficial grouping. Cyanophora is known from the abundant picoplankter in the low-latitude ocean plankton of shallow, productive calcareous lakes was not a Synechococcus,ashadbeen thitherto sup- (Whitton in John et al., 2002). posed, but another oxyphototrophic prokaryote Molecular investigation has revealed that the containing divinyl chlorophyll-a and -b pigments seemingly disparate algal phyla conform to one but nobilins (Chisholm et al., 1988, 1992); it was or other of two main lineages. The ‘green line’ named Prochlorococcus. The elucidation of a bio- of eukaryotes with endosymbiotic Cyanobacteria spheric role of a previously unrecognised organ- reflects the development of the chlorophyte and ism is achievement enough by itself (Pinevich euglenophyte phyla and to the important off- et al., 2000); for the organisms apparently to shoots to the bryophytes and the vascular plant occupy this transitional position in the evolu- phyla. The ‘red line’, with its secondary and even tion of plant life doubles the sense of scientific tertiary endosymbioses, embraces the evolution satisfaction. Nevertheless, subsequent investiga- of the rhodophytes, the chrysophytes and the tions of the phylogenetic relationships of the haptophytes, is of equal or perhaps greater fas- newly defined Prochlorobacteria, using immuno- cination to the plankton ecologist interested in logical and molecular techniques, failed to group diversity. Prochlorococcus with the other Prochlorales or even Akey distinguishing feature of the algae of to separate it distinctly from Synechococcus (Moore thegreen line is the inclusion of chlorophyll et al., 1998;Urbach et al., 1998). The present view b among the photosynthetic pigments and, typ- is that it is expedient to regard the Prochlorales ically, the accumulation of glucose polymers as aberrent Cyanobacteria (Lewin, 2002). (such as starch, paramylon) as the main prod- The common root of all eukaryotic algae and uct of carbon assimilation. The subdivision of higher plants is now understood to be based thegreen algae between the prasinophyte and upon original primary endosymbioses involv- thechlorophyte phyla reflects the evolutionary ing early eukaryote protistans and Cyanobacteria development and anatomic diversification within (Margulis, 1970, 1981). As more is learned about theline, although both are believed to have the genomes and gene sequences of microorgan- along history on the planet (∼1.5 Ga). Both isms, so the role of ‘lateral’ gene transfers in are also well represented by modern genera, in shaping them is increasingly appreciated (Doolit- water generally and in the freshwater phyto- tle et al., 2003). For instance, in terms of ultraplankton in particular. Of the modern prasino- structure, the similarity of 16S rRNA sequences, phyte orders, the Pedinomonadales, the Chloro- several common genes and the identical pho- dendrales and the Pyramimonadales each have tosynthetic proteins, all point to cyanobacterial significant planktic representation, in the sense 12 PHYTOPLANKTON

of producing populations of common occurrence cells, there is a striking variety of planktic and forming ‘blooms’ on occasions. Several mod- forms. ern chlorophyte orders (including Oedogoniales, Closest to the ancestral root are the cryp- Chaetophorales, Cladophorales, Coleochaetales, tophytes. These contain chlorophyll c2,aswell Prasiolales, Charales, Ulvales a.o.)are without as chlorophyll a and phycobilins, in plastid thy- modern planktic representation. In contrast, lakoids that are usually paired. Living cells are there are large numbers of volvocalean, chloro- generally green but with characteristic, species- coccalean and zygnematalean species in lakes specific tendencies to be bluish, reddish or and ponds and the Tetrasporales and Ulotrichales olive-tinged. The modern planktic representatives are also well represented. These show a very wide are exclusively unicellular; they remain poorly span of cell size and organisation, with flagel- known, partly because thay are not easy to lated and non-motile cells, unicells and filamen- identify by conventional means. However, about tous or ball-like coenobia, with varying degrees of 100species each have been named for marine mucilaginous investment and of varying consis- and fresh waters, where, collectively, they occur tency. The highest level of colonial development widely in terms of latitude, trophic state and is arguably in Volvox,inwhichhundreds of net- season. worked biflagellate cells are coordinated to bring Next comes the small group of single- about the controlled movement of the whole. celled flagellates which, despite showing similar- Colonies also reproduce by the budding off and ities with the cryptophytes, dinoflagellates and release of near-fully formed daughter colonies. euglenophytes, are presently distinguished in the The desmid members of the Zygnematales are phylum Raphidophyta. One genus, Gonyostomum, amongst the best-studied green plankters. Mostly is cosmopolitan and is found, sometimes in abun- unicellular, the often elaborate and beautiful dance, in acidic, humic lakes. The green colour architecture of the semi-cells invite the gaze and imparted to these algae by chlorophyll a is, to curiosity of the microscopist. some extent, masked by a xanthophyll (in this The euglenoids are unicellular flagellates. case, diatoxanthin) to yield the rather yellowish Amajorityofthe 800 or so known species pigmentation. This statement applies even more are colourless heterotrophs or phagotrophs and to theyellow-green algae making up the phyla are placed by zoologists in the protist order Xanthophyta and Eustigmatophyta. The xantho- Euglenida. Molecular investigations reveal them phytes are varied in form and habit with a to be a single, if disparate group, some of which number of familiar unicellular non-flagellate or acquired the phototrophic capability through biflagellate genera in the freshwater plankton, as secondary symbioses. It appears that even the well as the filamentous Tribonema of hard-water phototrophic euglenoids are capable of absorb- lakes. The eustigmatophytes are unicellular coc- ing and assimilating particular simple organic coid flagellates of uncertain affinities that take solutes. Many of the extant species are associ- their name from the prominent orange eye-spots. ated with organically rich habitats (ponds and The golden algae (Chrysophyta) represent a lagoons, lake margins, sediments). further recombination along the red line, giv- The ‘red line’ of eukaryotic evolution is based ing rise to a diverse selection of modern unicel- on rhodophyte plastids that contain phycobilins lular, colonial or filamentous algae. With a dis- and chlorophyll a,and whose single thylakoids tinctive blend of chlorophyll a, c1 and c2,andthe lie separately and regularly spaced in the plastid major presence of the xanthophyll fucoxanthin, stroma (see, e.g., Kirk, 1994). The modern phy- the chrysophytes are presumed to be close to lum Rhodophyta is well represented in marine thePhaeophyta, which includes all the macro- (especially; mainly as red seaweeds) and fresh- phytic brown seaweeds but no planktic vege- water habitats but no modern or extinct plank- tative forms. Most of the chrysophytes have, tic forms are known. However, among the inter- in contrast, remained microphytic, with numer- esting derivative groups that are believed to ous planktic genera. A majority of these come owetosecondary endosymbioses of rhodophyte from fresh water, where they are traditionally THE DIVERSIFICATION OF PHYTOPLANKTON 13 supposed to indicate low nutrient status and pro- is a prominent thread, as long as the cell; in oth- ductivity (but see Section 3.4.3:theymaysimply ers it is smaller or even vestigial but, in most be unable to use carbon sources other than car- instances, can be bent or coiled. Most of the bon dioxide). Mostly unicellular or coenobial flag- known extant haptophyte species are marine; ellates, many species are enclosed in smooth some genera, such as Chrysochromulina,arerep- protective loricae, or they may be beset with resented by species that are relatively frequent numerous delicate siliceous scales. The group has members of the plankton of continental shelves been subject to considerable taxonomic revision and of mesotrophic lakes. Phaeocystis is another and reinterpretation of its phylogenies in recent haptophyte common in enriched coastal waters, years. The choanoflagellates (formerly Craspedo- where it may impart a visible yellow-green colour phyceae, Order Monosigales) are no longer con- to thewater at times, and give a notoriously slimy sidered to be allied to the Chrysophytes. texture to the water (Hardy, 1964). The last three phyla named in Table 1.1, The coccolithophorids are exclusively marine each conspicuously represented in both limnetic haptophytes and among the most distinctive and marine plankton – indeed, they are the microorganisms of the sea. They have a charac- main pelagic eukaryotes in the oceans – are teristic surface covering of coccoliths – flattened, also remarkable in having relatively recent ori- often delicately fenestrated, scales impregnated gins, in the mesozoic period. The Bacillariophyta with calcium carbonate. They fossilise particu- (the diatoms) is a highly distinctive phylum of larly well and it is their accumulation which single cells, filaments and coenobia. The char- mainly gave rise to the massive deposits of chalk acteristics are the possession of golden-brown that gave its name to the Cretaceous (from Greek plastids containing the chlorophylls a, c1 and kreta,chalk) period, 120–65 Ma BP. Modern coc- c2 and the accessory pigment fucoxanthin, and colithophorids still occur locally in sufficient pro- the well-known presence of a siliceous frustule fusion to generate ‘white water’ events. One of or exoskeleton. Generally, the latter takes the thebest-studied of the modern coccolithophorids form of a sort of lidded glass box, with one of is Emiliana. two valves fitting in to the other, and bound by The final group in this brief survey is the one or more girdle bands. The valves are often dinoflagellates. These are mostly unicellular, patterned with grooves, perforations and callosi- rarely colonial biflagellated cells; some are rel- ties in ways that greatly facilitate identification. atively large (up to 200 to 300 µm across) and Species are ascribed to one or other of the two have complex morphology. Pigmentation gener- main diatom classes. In the Biddulphiales, or ally, but not wholly, reflects a red-line ancestry, centric diatoms, the valves are usually cylindri- the complex plastids containing chlorophyll a, cal, making a frustule resembling a traditional c1 and c2 and either fucoxanthin or peridinin pill box; in the Bacillariales, or pennate diatoms, as accessory pigments, possibly testifying to ter- the valvesareelongatebutthegirdles are short, tiary endosymbioses (Delwiche, 2000). The group having the appearance of the halves of a date shows an impressive degree of adaptive radia- box. While much is known and has been writ- tion, with naked gymnodinioid nanoplankters ten ontheirmorphology and evolution (see, for through to large, migratory gonyaulacoid swim- instance, Round et al., 1990), the origin of the mers armoured with sculpted plates and to deep- siliceous frustule remains obscure. watershade forms with smooth cellulose walls The Haptophyta are typically unicellular gold such as Pyrocystis. Some genera are non-planktic or yellow-brown algae, though having amoeboid, and even pass part of the life cycle as epiphytes. coccoid or palmelloid stages in some cases. The Freshwater species of Ceratium and larger species pigment blend of chlorophylls a, c1 and c2, of Peridinium are conspicuous in the plankton with accessory fucoxanthin, resembles that of of certain types of lakes during summer strati- other gold-brown phyla. The haptophytes are dis- fication, while smaller species of Peridinium and tinguished by the possession of a haptonema, other genera (e.g. Glenodinium)are associated with located between the flagella. In some species it mixed water columns of shallow ponds. 14 PHYTOPLANKTON

Figure 1.1 Non-motile unicellular phytoplankters. (a) Synechococcus sp.; (b) Ankyra judayi; (c) Stephanodiscus rotula; (d) Closterium cf. acutum. Scale bar, 10 µm. Original photomicrographs by Dr H. M. Canter-Lund, reproduced from Reynolds (1984a).

The relatively recent appearance of diatoms, 10–11 ◦C). Life on Earth suffered a severe set- coccolithophorids and dinoflagellates in the back, perhaps as close as it has ever come fossil record provides a clear illustration of to total eradication. In a period of less than how evolutionary diversification comes about. 0.1 Ma, many species fell extinct and the sur- Although it cannot be certain that any of these vivors were severely curtailed. As the planet three groups did not exist beforehand, there cooled over the next 20 or so million years, is no doubt about their extraordinary rise dur- the rump biota, on land as in water, were able ing the Mesozoic. The trigger may well have to expand and radiate into habitats and niches been the massive extinctions towards the end of that were otherwise unoccupied (Falkowski, the Permian period about 250 Ma BP, when a 2002). huge release of volcanic lava, ash and shroud- Dinoflagellate fossils are found in the early ing dust from what is now northern Siberia Triassic, the coccolithophorids from the late Tri- brought about a world-wide cooling. The trend assic (around 180 Ma BP). Together with the wasquickly reversed by accumulating atmo- diatoms, many new species appeared in the Juras- spheric carbon dioxide and a period of severe sic and Cretaceous periods. In the sea, these three global warming (which, with positive feedback groups assumed a dominance over most other of methane mobilisation from marine sediments, forms, the picocyanobacteria excluded, which raised ambient temperatures by as much as persists to the present day. GENERAL FEATURES OF PHYTOPLANKTON 15

Figure 1.2 Planktic unicellular ﬂagellates. (a) Two variants of Ceratium hirundinella; (b) overwintering cyst of Ceratium hirundinella, with vegetative cell for comparison; (c) empty case of Peridinium willei to show exoskeletal plates and ﬂagellar grooves; (d) Mallomonas caudata; (e) Plagioselmis nannoplanctica; (f) two cells of Cryptomonas ovata; (g) Phacus longicauda; (h) Euglena sp.; (j) Trachelomonas hispida. Scale bar, 10 µm. Original photomicrographs by Dr H. M. Canter-Lund, reproduced from Reynolds (1984a).

whether they occurred among other precursors 1.4 General features of that subsequently established new lines of plank- phytoplankton tic invaders. It is not a problem that can yet be answered satisfactorily. However, it does not detract from Despite being drawn from a diverse range of thefact that to function and survive in the what appear to be distantly related phyloge- plankton does require some specialised adapta- netic groups (Table 1.1), there are features that tions. It is worth emphasising again that just as phytoplankton share in common. In an earlier phytoplankton comprises organisms other than book (Reynolds, 1984a), I suggested that these algae, so not all algae (or even very many of features reﬂected powerful convergent forces in them) are necessarily planktic. Moreover, neither evolution, implying that the adaptive require- theshortness of the supposed step to a plank- ments for a planktic existence had risen inde- tic existence nor the generally low level of struc- pendently within each of the major phyla repre- tural complexity of planktic unicells and coeno- sented. This may have been a correct deduction, bia should deceive us that they are necessarily although there is no compelling evidence that simple organisms. Indeed, much of this book it is so. On the other hand, for small, unicellu- deals with the problems of life conducted in a lar microorganisms to live freely in suspension ﬂuid environment, often in complete isolation in water is an ancient trait, while the transition from solid boundaries, and the often sophisti- toafullplankticexistence is seen to be a rel- cated means by which planktic organisms over- atively short step. It remains an open question come them. Thus, in spite of the diversity of phy- whether the supposed endosymbiotic recombina- logeny (Table 1.1), even a cursory consideration tions could have occurred in the plankton, or of the range of planktic algae (see Figs. 1.1–1.5) 16 PHYTOPLANKTON

Figure 1.3 Coenobial phytoplankters. Colonies of the diatoms (a) Asterionella formosa, (b) Fragilaria crotonensis and (d) Tabellaria ﬂocculosa var. asterionelloides. The fenestrated colony of the chlorophyte Pediastrum duplex is shown in (c). Scale bar, 10 µm. Original photomicrographs by Dr H. M. Canter-Lund, reproduced from Reynolds (1984a).

reveals a commensurate diversity of form, func- of immediate respiratory needs (Chapter 3). How- tion and adaptive strategies. ever, radiant energy of suitable wavelengths What features, then, are characteristic and (photosynthetically active radiation,orPAR)isnei- common to phytoplankton, and how have they ther universally or uniformly available in water been selected? The overriding requirements of but is sharply and hyperbolically attenuated with any organism are to increase and multiply its depth, through its absorption by the water and kind and for a sufficient number of the progeny scattering by particulate matter (to be discussed to survive for long enough to be able to invest in Chapter 3). The consequence is that for a in the next generation. For the photoautotroph, given phytoplankter at anything more than a this translates to being able to fix sufficient car- few metersindepth,thereislikely to be a crit- bon and build sufficient biomass to form the ical depth (the compensation point)below which next generation, before it is lost to consumers net photosynthetic accumulation is impossible. or to any of the several other potential fates that It follows that the survival of the phytoplankter await it. For the photoautotroph living in water, depends upon its ability to enter or remain in the important advantages of archimedean sup- theupper, insolated part of the water mass for port and the temperature buffering afforded by at least part of its life. the highspecific heat of water (for more, see This much is well understood and the point Chapter 2)mustbebalanced against the diffi- has been emphasised in many other texts. These cuties of absorbing sufficient nutriment from have also proffered the view that the essential often very dilute solution (the subject of Chapter characteristic of a planktic photoautotroph is to 4)andofintercepting sufficient light energy to minimise its rate of sinking. This might be liter- sustain photosynthetic carbon fixation in excess ally true if the water was static (in which case, GENERAL FEATURES OF PHYTOPLANKTON 17

Figure 1.4 Filamentous phytoplankters. Filamentous coenobia of the diatom Aulacoseira subarctica (a, b; b also shows a spherical auxospore) and of the Cyanobacteria (c) Gloeotrichia echinulata, (d) Planktothrix mougeotii, (e) Limnothrix redekei (note polar gas vacuoles), (f) Aphanizomenon ﬂos-aquae (with one akinete formed and another differentiating) and Anabaena ﬂos-aquae (g) in India ink, to show the extent of mucilage, and (h) enlarged, to show two heterocysts and one akinete. Scale bar, 10 µm. Original photomicrographs by Dr H. M. Canter-Lund, reproduced from Reynolds (1984a).

neutral buoyancy would provide the only ideal Toagreater or lesser degree, these move- adaptation). However, natural water bodies are ments of the medium overwhelm the sinking tra- almost never still. Movement is generated as a jectories of phytoplankton. The traditional view consequence of the water being warmed or cool- of planktic adaptations as mechanisms to slow ing, causing convection with vertical and hori- sinking rate needs to be adjusted. The essential zontal displacements. It is enhanced or modiﬁed requirement of phytoplankton is to maximise the by gravitation, by wind stress on the water sur- opportunities for suspension in the various parts face and by the inertia due to the Earth’s rotation of the eddy spectrum. In many instances, the (Coriolis’ force). Major ﬂows are compensated by adaptations manifestly enhance the entrainabil- return currents at depth and by a wide spectrum ity of planktic organisms by turbulent eddies. of intermediate eddies of diminishing size and These include small size and low excess den- of progressively smaller scales of turbulent diffu- sity (i.e. organismic density is close to that of sivity, culminating in molecular viscosity (these water, ∼1000 kg m−3), which features do con- motions are characterised in Chapter 2). tribute to a slow rate of sinking. They also include 18 PHYTOPLANKTON

Figure 1.5 Colonial phytoplankters. Motile colonies of (a) Volvox aureus, with (b) detail of cells, (c) Eudorina elegans, (d) Uroglena sp. and (e) Dinobryon divergens; and non-motile colonies, all mounted in India ink to show the extent of mucilage, of (f) Microcystis aeruginosa, (g) Pseudosphaerocystis lacustris and (h) Dictyosphaerium pulchellum. Scale bar, 10 µm. Original photomicrographs by Dr H. M. Canter-Lund, reproduced from Reynolds (1984a).

mechanisms for increasing frictional resistance isms of the nekton, – cephalopods, ﬁsh, reptiles with the water, independently of size and dens- and mammals – which are able to direct their ity. At the same time, other phytoplankters show ownmovements to overcome a still broader range adaptations that favour disentrainment, at least of the pelagic eddy spectrum. from weak turbulence, coupled with relatively All these aspects of turbulent entrainment large size (often achieved by colony formation), and disentrainment are explored more deeply streamlining and an ability to propel themselves and more empirically in Chapter 2.Forthe rapidly through water. Such organisms exploit a moment, it is important to understand how they different part of the eddy spectrum from the ﬁrst impinge upon phytoplankton morphology in a group. The principle extends to the larger organ- general sense. GENERAL FEATURES OF PHYTOPLANKTON 19

1.4.1 Size and shape These traits are represented and sometimes Apart from the issue of suspension, there is blended in the morphological adaptations of spe- a further set of constraints that resists large cific plankters. They can be best illustrated by size among phytoplankters. Autotrophy implies a the plankters themselves and by examining how requirement for inorganic nutrients that must be they influence their lives and ecologies. The wide absorbed from the surrounding medium. These ranges of form, size, volume and surface area are generally so dilute and so much much less are illustrated by the data for freshwater plank- concentrated than they have to be inside the ton presented in Table 1.2. The list is an edited, plankter’s cell that uptake is generally against a simplified and updated version of a similar table very steep concentration gradient that requires in Reynolds (1984a) which drew on the author’s theexpenditure of energy to counter it. Once ownmeasurements but quoted from other com- inside the cell, the nutrient must be translo- pilations (Pavoni, 1963;Nalewajko, 1966;Besch et cated to the site of its deployment, invoking dif- al., 1972; Bellinger, 1974;Findenegg, Nauwerck fusion and transport along internal molecular in Vollenweider, 1974;Willén, 1976;Bailey-Watts, pathways. Together, these twin constraints place 1978;Trevisan, 1978). The sizes are not precise ahighpremiumon short internal distances: and are often variable within an order of mag- cells that are absolutely small or, otherwise, nitude. However, the listing spans nearly eight have one or two linear dimensions truncated (so orders, from the smallest cyanobacterial unicells that cells are flattened or are slender) benefit of ∼1 µm3 or less, the composite structures of from this adaptation. Conversely, simply increas- multicellular coenobia and filaments with vol- ing the diameter (d)ofasphericalcellisto umes ranging between 103 and 105 µm3,through increase the constraint for, though the surface to unitsof>106 µm3 in which cells are embedded area increases in proportion to d2,thevolume within a mucilaginous matrix. Indeed, the list is increases with d3.However,distortionfromthe conservative in so far as colonies of Microcystis of spherical form, together with surface convolu- >1mmindiameter have been observed in nature tion, provides a way of increasing surface in (author’s observations; i.e. up to 109 µm3 in vol- closer proportion to increasing volume, so that ume). Because all phytoplankters are ‘small’ in the latterisenclosedbyrelatively more sur- human terms, requiring good microscopes to see face than the geometrical minimum required them, it is not always appreciated that the nine to bound the same volume (a sphere). In this or more orders of magnitude over which their respect, the adaptive requirements for maximis- sizes range is comparable to that spanning forest ing entrainability and for enhancing the assim- trees to the herbs growing at their bases. Like the ilation of nutrients taken up across the surface example, the biologies and ecologies of the indi- coincide. vidual organisms vary considerably through the It is worth adding, however, that nutrient spectrum of sizes. uptake from the dilute solution is enhanced if the medium flows over the cell surface, dis- 1.4.2 Regulating surface-to-volume ratio placing that which may have already become Dwelling on the issue of size and shape, we will depleted. Movement of the cell relative to the find, as already hinted above, that a good deal adjacent water achieves the similar effect, with of plankton physiology is correlated to the ratio measurable benefit to uptake rate (Pasciak and of the surface area of a unit (s)toitsvolume Gavis, 1974;but see discussion in Section 4.2.1). (v). ‘Unit’ in this context refers to the live habit It may be hypothesised that it is advantageous of the plankter: where the vegetative form is for the plankter not to achieve isopycnic suspen- unicellular (exemplified by the species listed in sion in the water but to retain an ability to sink Table 1.2A), it is only the single cell that interacts or float relative to the immediate surroundings, with its environment and is, plainly, synonymous regardless of the rate and direction of travel of with the ‘unit’. If cells are joined together to the latter, just to improve the sequestration of comprise a larger single structure, for whatever nutrients. advantage, then the individual cells are no longer 20 PHYTOPLANKTON

Ta b l e 1.2 Nominal mean maximum linear dimensions (MLD), approximate volumes (v) and surface areas (s)ofsome freshwater phytoplankton

MLD vss/v Species Shape (µm) (µm3)(µm2)(µm−1) (A) Unicells Synechoccoccus ell ≤ 418 35 1.94 (1–20) Ankyra judayi bicon 16 24 60 2.50 (3–67) Monoraphidium grifﬁthsii cyl 35 30 110 3.67 Chlorella pyrenoidosa sph 4 33 50 1.52 (8–40) Kephyrion littorale sph 5 65 78 1.20 Plagioselmis ell 11 72 108 1.50 nannoplanctica (39–134) Chrysochromulina parva cyl 6 85 113 1.33 Monodus sp. ell 8 105 113 1.09 Chromulina sp. ell 15 440 315 0.716 Chrysococcus sp. sph 10 520 315 0.596 Stephanodiscus cyl 11 600 404 0.673 hantzschii (180–1 200) Cyclotella praeterissima cyl 10 760 460 0.605 (540–980) Cyclotella meneghiniana cyl 15 1 600 780 0.488 Cryptomonas ovata ell 21 2710 1 030 0.381 (1 950–3 750) Mallomonas caudata ell 40 4 200 3 490 0.831 (3 420–10 000) Closterium aciculare bicon 360 4 520 4 550 1.01 Stephanodiscus rotula cyl 26 5 930 1 980 0.334 (2 220–18 870) Cosmarium depressum (a)247780 2 770 0.356 (400–30 000) Synedra ulna bicon 110 7 900 4 100 0.519 Staurastrum pingue (b)909450 6 150 0.651 (4 920–16 020) Ceratium hirundinella (c) 201 43 740 9 600 0.219 (19 080–62 670) Peridinium cinctum ell 55 65 500 7 070 0.108 (33 500–73 100) (B) Coenobia Dictyosphaerium (d )40 900 1 540 1.71 pulchellum (40 cells) Scenedesmus (e)801000 908 0.908 quadricauda (4 cells) Asterionella formosa (f ) 130 5 160 6 690 1.30 (8 cells) (4 430–6 000) (cont.) GENERAL FEATURES OF PHYTOPLANKTON 21

Ta b l e 1.2 (cont.)

MLD vss/v Species Shape (µm) (µm3)(µm2)(µm−1) Fragilaria crotonensis (g)706230 9 190 1.48 (10 cells) (4 970–7 490) Dinobryon divergens (h) 145 7 000 5 350 0.764 (10 cells) (6 000–8 500) Tabellaria ﬂocculosa var. (f )9613800 9 800 0.710 asterionelloides (6 520–13 600) (8 cells) Pediastrum boryanum ( j) 100 16 000 18 200 1.14 (32 cells) (C) Filaments Aulacoseira subarctica cyl (k) 240 5 930 4 350 0.734 (10 cells) (4 740–7 310) Planktothrix mougeotii cyl (k) 1000 46 600 24 300 0.521 (1 mm length) Anabaena circinalis (m)602040 2 110 1.03 (20 cells) (n)7529000 6 200 0.214 Aphanizomenon (p) 125 610 990 1.62 ﬂos-aquae (50 cells) (q) 125 15 400 5 200 0.338 (D) Mucilaginous colonies Coenochloris fottii sph 46 51 × 103 6.65 × 103 0.13 (cells 80–1200 µm3) Eudorina unicocca sph 130 1.15 × 106 53.1 × 103 0.046 (cells 120–1200 µm3) Uroglena lindii sph 160 2.2 × 106 81 × 103 0.037 (cells 100 µm3) Microcystis aeruginosa sph 200 4.2 × 106 126 × 103 0.030 (cells 30–100 µm3) Volvox globator sph (r) 450 47.7 × 106 636 × 103 0.013 (cells ∼ 60 µm3)(s) 450 6.4 × 106 636 × 103 0.099

Notes: The volumes and surface areas are necessarily approximate. The values cited are those adopted and presented in Reynolds (1984a); some later additions taken from Reynolds (1993a), mostly based on his own measurements. The volumes given in brackets cover the ranges quoted elsewhere in the literature (see text). Note that the volumes and surface areas are calculated by analogy to the nearest geometrical shape. Surface sculpturing is mostly ignored. Shapes considered include: sph (for a sphere), cyl (cylinder), ell (ellipsoid), bicon (two cones fused at their bases, area of contact ignored from surface area calculation). Other adjustments noted as follows: a Cell visualised as two adjacent ellipsoids, area of contact ignored. b Cell visualised as two prisms and six cuboidal arms, area of contact ignored. c Cell visualised as two frusta on elliptical bases, two cylindrical (apical) and two conical (lateral) horns. d Coenobium envisaged as 40 contiguous spheres, area of contact ignored. e Coenobium envisaged as four adjacent cuboids, volume of spines ignored f Coenobium envisaged as eight cuboids, area of contact ignored. 22 PHYTOPLANKTON

Notes to Table 1.2 (cont.) g Each cell visualised as four trapezoids; area of contact between cells ignored. h Coenobium envisaged as a seies of cones, area of contact ignored j Coenobium envisaged as a discus-shaped sphaeroid. k Coenobium envisaged as a chain of cylinders, area of contact between cells ignored. l Coenobium envisaged as a single cylinder, terminal taper ignored. m Filament visualised as a chain of spheres, area of contact between them ignored n Filament visualised as it appears in life, enveloped in mucilage, turned into a complete ‘doughnut’ ring, with a cross-sectional diameter of 21 µm. p Filament visualised as a chain of ovoids, area of contact between them ignored. q For the typical ‘raft’ habit of this plankter, a bundle of ﬁlaments is envisaged, having an overall length of 125 µm and a diameter of 12.5 µm. r The volume calculation is based on the external dimensions. s In fact the cells in the vegetative stage are located exclusively on the wall of a hollow sphere. This second volume calculation supposes an average wall thickness of 10 µm and subtracts the hollow volume.

independent but rather constitute a multicellular ‘unit’ whose behaviour and experienced envi- 107 ronment is simultaneously shared by all the others in the unit. Such larger structures may deploy cells either in a plate- or ball-like coenobium (exem- pliﬁed by the species listed in Table 1.2B) or, end- 106 to-end, to make a uniseriate filament (Table 1.2C). Generally, added complexity brings increased size but, as volume increases as the cube but surface 5 as the square of the linear dimension, there is 10

natural tendency to sacrifice a high surface-to- 2 µ m volume ratio. / s However, a counteractive tendency is found 104 among the coenobial and filamentous units (and also among larger unicells), in which increased Nominal size is accompanied by increased departure from the spherical form. This means, in large-volume 103 units, more surface bounds the volume than the strict geometrical minimum provided by the sphere. In addition to distortion, surface fold- 102 Geometrically excluded ing, the development of protuberances, lobes and horns all contribute to providing more surface for not much more volume. The trend is shown in Fig. 1.6,inwhichthesurface areas of the 3 5 7 species listed in Tables 1.2A, B and C are plot- 01010 10 10 Nominal v (µm3) ted against the corresponding, central-value volumes, in log/log format. The smaller spherical Figure 1.6 Log/log relationship between the surface areas and ovoid plankters are seen to lie close to the (s) and volumes (v)ofselected freshwater phytoplankters (lower) slope representing the geometric mini- shown in Table 1.2. The lower line is fitted to the points mum of surface on volume, s ∝ v,butprogres- ()referring to species forming quasi-spherical mucilaginous sively larger units drift away from it. The sec- coenobia (log s = 0.67 log v + 0.7); the upper line is the ond regression, fitted to the plotted data, has a regression of coenobia (log s = 0.82 log v + 0.49) fitted to all t steeper gradient of v0.82. The individual values of other points ( ). Redrawn from Reynolds (1984a). GENERAL FEATURES OF PHYTOPLANKTON 23 s/v entered in Table 1.2BandCshowseveral examples of algal units having volumes of between 103 1000 and 105 µm3 but maintaining surface-to-volume ratios of >1. In the case of Asterionella,theslen- der individual cuboidal cells are distorted in one C plane and are attached to their immediate coeno-

− 1 100 bial neighbours by terminal pads representing S averysmallpart of the total unit surface. The resultant pseudostellate coenobium is actually MLD / µ m a flattened spiral. In Fragilaria crotonensis,astill 10 Geometrically greater s/v ratio is achieved. Though superficially excluded similar to those of Asterionella,itscells are widest in their mid-region and where they link, mid- valve to mid-valve, to their neighbours to form the‘double comb’ appearance that distinguishes 00.10.01 110 this species from others (mostly non-planktic) of Nominal s/v ( µm−1) the same genus. Among the filamentous forms, there isawidespread tendency for cells to be Figure 1.7 The shapes of phytoplankters: log/log plot of elongated in one plane and to be attached to maximum linear dimension (MLD) versus nominal s/v of their neighbours at their polar ends so that individual phytoplankters (data in Table 1.2). Similar the long axesarecumulated (e.g. in Aulacoseira, morphologies are grouped together (I, spherical cells; II, spherical colonies; III, squat ellipsoids and cylinders, of which Fig. 1.4). IV are exclusively centric diatoms; V, attenuate cells and Again confining the argument to the planktic filaments; VI, coenobia; VII, bundles of filaments of Anabaena forms covered in Tables 2.2A, B and C, whose vol- or Aphanizomenon);C(forCeratium) and S (for Staurastrum) umes, together, cover five orders of magnitude, identify shapes with large protuberances). The vertical dotted these show surface-to-volume ratios that fall in lines define the distributions of most marine phytoplankters scarcely more than one-and-a-half orders (3.6 to according to Lewis (1976). Redrawn from Reynolds (1984a). 0.1). This evident conservatism of the surface-to- volume ratio among phytoplankton was noted in amemorable paper by Lewis (1976). He argued that this is not a geometric coincidence but an represented these modifications by plotting the evolutionary outcome of natural selection of the maximum linear dimension (MLD) of the unit adaptations for a planktic existence. Thus, how- against its surface-to-volume ratio. His approach ever strong is the selective pressure favouring is followed in the construction of Fig. 1.7,in increased size and complexity, the necessity to which the relevant data from Table 1.2 are plot- maintain high s/v, whether for entrainment or ted. The diagonal line is a geometric boundary, nutrient exchange or both, remains of overriding representing the diminution of s/v of spheres importance. In other words, the relatively rigid against the increment in diameter and, indeed, constraints imposed by maintenance of an opti- upon which the spherical unicells (marked I) mum surface-to-volume ratio constitute the most and colonies (II) are located. All other shapes fall influential single factor governing the shape of above this line, the further above it being the planktic algae. more distorted with respect to the sphere of the Lewis (1976)developed this hypothesis same MLD. The broken dotted lines bound the through an empirical analysis of phytoplankton s/v ratios of non-spherical forms. All the ellipsoid shapes. To a greater or lesser extent, departure shapes (III, such as Mallomonas, Rhodomonas), from the spherical form through the provision squat cylinders (IV, including Cyclotella and of additional surface area is achieved by shape Stephanodiscus spp.), attenuated needle-like cells attenuation in one or, perhaps, two planes, and filaments (V: Monoraphidium, Closterium, respectively resulting in slender, needle-like Aulacoseira, Planktothrix)fall within this area. So formsorflattened, plate-like structures. Lewis do the coenobial forms comprising individual 24 PHYTOPLANKTON

attenuated cells (VI, e.g. Asterionella, Fragilaria) Cyanobacteria included in Table 1.2 (Anabaena and the unicells with significant horn-like circinalis, Aphanizomenon flos-aquae), the supposed or arm-like distortions (Ceratium, Staurastrum, advantage of the filamentous habit is sacrificed individually identified). The plot backs the asser- through a combination of aggregation, coiling tion that the attractive and sometimes bizarre and mucilage production to the attainment of forms adopted by planktic freshwater algae are rapid rates of migration (Booker and Walsby, functionally selected. 1979). Provided colonies have a simultaneous capac- 1.4.3 Low surface-to-volume ratio: ity for controlled motility, there are good tele- mucilaginous forms ological grounds for deducing circumstances The principle of morphological conservation of a when massive provision of mucilage represents favourable surface-to-volume ratio, which holds adiscrete and alternative adaptation to a plank- equally for the phytoplankton of marine and tic existence. However, the idea that streamlin- inland waters, might be more strongly coming is more than a fortuitous benefit is chal- pelling were it not for the fact that another lenged by the many non-motile species that exist common evolutionary trend – that of embedding as mucilaginous colonies. There are other demon- vegetative cells in swathes of mucilage – repre- strable benefits from a mucilaginous exterior, sents a total antithesis. The formation of globu- including defence against fungal attack, grazers, lar colonies is prevalent among the freshwater digestion or metal toxicity, and there are circum- Cyanobacteria, Chlorophyta and the Chryso- stances in which it might assist in the sequestra- phyta. It is also observed in the vegetative tion or storage of nutrients or in protecting cells life-history stages of the haptophyte, Phaeocys- from an excessively oxidative environment (see tis,though, generally, the trait is not com- Box 6.1, p. 271). Even mucilage itself, essentially mon among the marine phytoplankton. In many amatrix of hygroscopic carbohydrate polymers instances, the secondary structures are predom- immobilising relatively large amounts of water, inantly mucilaginous and the live cells may is highly variable in its consistency, intraspecifi- occupy as little as 2% of the total unit volume cally as well as interspecifically. in Coenochloris and Uroglena and scarcely exceeds Thus, doubts persist about the true function 20% in Microcystis or Eudorina.Itwasoriginally of mucilage investment. However, a consistent supposed to provide a low-density buoyancy aid geometric consequence of mucilage investment but it has since been shown that any advantage is that the planktic unit is left with an excep- is quickly lost to increased size (see Chapter 2). In tionally low surface-to-volume ratio (i.e. area II, some instances, the individual cells are flagellate towards the left in Fig. 1.7). (as in Uroglena and Eudorina)andtheflagella pass through the mucilage to the exterior, where their coordinated beating propels the whole colony 1.5 The construction and through the medium. Because the surface offers composition of freshwater little friction, the mucilage is said to be helpful in assisting rapid passage and migration through phytoplankton weakly turbulent water. Certainly, in the case of the colonial gas-vacuolate Cyanobacteria that The architecture of the cells of planktic algae con- are able to regulate their buoyancy (e.g. Micro- formstoabasic model, common to the major- cystis, Snowella, Woronichinia), larger colonies float ity of eukaryotic plants. A series of differenti- more rapidly than smaller ones of the same den- ated protoplasmic structures are enclosed within sity (Reynolds, 1987a). Merely adjusting buoyancy avitalmembrane, the plasmalemma. This mem- then becomes a potentialy effective means of brane is complex, comprising three or four dis- recovering or controlling vertical position in the tinct layers. In a majority of algae there is a fur- water (Ganf, 1974a). It is interesting that, in the ther, non-living cell wall,made of cellulose or two buoyancy-regulating filamentous species of other, relatively pure, condensed carbohydrate THE CONSTRUCTION AND COMPOSITION OF FRESHWATER PHYTOPLANKTON 25 polymer, such as pecten. Among some algal too, is multilayered but has the distinctive bac- groups, the wall may be more or less impreg- terial configuration. The cells lack a membrane- nated with inorganic deposits of calcium car- bound nucleus and plastids, the genetic material bonate or silica. High-power scanning electron and photosynthetic thylakoid membranes being microscopy reveals that these deposits can form unconfined through the main body (stroma) of amore or less continuous but variably thick- thecell. The pigments, chlorophyll and accessory ened and fenestrated surface (as in the siliceous phycobilins, colour the whole cell. Glycogen is frustule wall of diatoms) or can comprise an theprincipal photosynthetic condensate and pro- investment of individual scales (like those of the teinaceous structured granules may also be accu- Synurophyceae, made of silica, or of the coccol- mulated. Many planktic genera contain, poten- ithophorids, made of carbonate). These exoskele- tially or actually, specialised intracellular pro- tons are distinctive and species-diagnostic. Some teinaceous gas-filled vacuoles which may impart algae lack a polymer wall and are described as buoyancy to the cell. ‘naked’. Both naked and walled cells may carry From an ecological point of view, the ultra- an additional layer of secreted mucilage. structural properties of phytoplankton cells The intracellular protoplasm (cytoplasm) is assume considerable relevance to the resource generally a viscous, gel-like suspension in which requirements of their assembly, as well as to the nucleus, one or more plastids and vari- adaptive behaviour, productivity and dynamics ous other organelles, including the endoplas- of populations. Thus, it is important to establish mic reticulum and the mitochondria, and some anumber of empirical criteria of cell composi- condensed storage products are maintained. The tion that impinge upon the fitness of individ- plastids vary hugely and interspecifically in ual plankters and the stress thresholds relative shape – from a solitary axial cup (as in the to light, temperature and nutrient availability. Volvocales), numerous discoids (typical of cen- These include methods for assessing the biomass tric diatoms), one or two broad parietal or of phytoplankton populations and the environ- axial plates (as in Cryptophytes) or more com- mental capacity to support them. plex shapes (many desmids). All take on the intense coloration of the dominant photosyn- 1.5.1 Dry weight thetic pigments they contain – chlorophyll a Characteristically, the major constituent of the and β-carotene and, variously, other chlorophylls live plankter is water. If the organism is air-dried and/or accessory xanthophylls. The stored con- to remove all uncombined water, the residue densates of anabolism are also conspicuously will comprise both organic (mainly protoplasm variable among the algae: starch in the chloro- and storage condensates) and inorganic (such as phytes and cryptophytes, other carbohydrates the carbonate or silica impregnated into the cell in the euglenoids (paramylon) and the Chryso- walls) fractions. Oxidation of the organic frac- phyceae, oils in the Xanthophyceae). Many also tion, by further heating in air to ∼500 ◦C, yields store protein in the cytoplasm. The quantities of an ash approximating to the original inorganic all storage products vary with metabolism and constituents. The relative masses of the ash and environmental circumstances. ash-free (i.e. organic) fractions of the original Intracellular vacuoles are to be found in most material may then be back-calculated. planktic algae but the large sap-filled spaces char- The dry weights and the ash contents of a acteristic of higher-plant cells are relatively rare, selection of freshwater phytoplankton are pre- other than in the diatoms. Osmoregulatory con- sented in Table 1.3.Generally, cell dry mass tractile vacuoles occur widely, though not univer- (Wc)increases with increasing cell volume (v), sally, among the planktic algae, varying in num- as shown inFig.1.8. The regression, fitted to ber and distribution among the phylogenetic all data points, has the equation Wc = 0.47 groups. v0.99,with a high coefficient of correlation (0.97). The prokaryotic cell of a planktic Cyanobac- At first sight, the relationship yields the useful terium is also bounded by a plasmalemma. It, general prediction that the dry weights of live 26 PHYTOPLANKTON

Ta b l e 1.3 Air-dry weights, ash-free free dry weights, chlorophyll content and volume of individual cellsa from natural populations (all values are means of collected data having considerable ranges of variability)

Ash-free dry Dry weight weight Chla Volume Species (pg cell−1) (pg cell−1) Ash % dry (pg cell−1)(µm3 cell−1) Cyanobacteria Anabaena circinalisb 45 – – 0.72 99 Aphanizomenon flos-aquaeb 3.9 – – 0.04 8.2 Microcystis aeruginosab 32 – – 0.36 73 Planktothrix mougeotiia,b 28000 – – 243 46 600 Chlorophytes Ankyra judayib –– –0.45 24 Chlorella pyrenoidosab 15 – – 0.15 33 Chlorella pyrenoidosac 5.1–6.4 4.5–5.7 11.4 – 20 Closterium aciculareb –– –894520 Eudorina elegansb 273 – – 5.5 320 Eudorina elegansc 251–292 233–268 7.9 – 320 Eudorina unicoccab –– –9.5 586 Monoraphidium contortumc 5.2–5.7 4.7–5.0 10.4 – 30 Scenedesmus quadricaudac 99–104 91–95 8.5 200 Staurastrum pingueb –– –579450 Staurastrum sp.c 4680–4940 4480–4620 5.3 – 20 500 Volvox aureusb 99 – – 1.1 60 Diatoms Asterionella formosab 292–349 – – 1.8 554–736 Asterionella formosac 243–291 104–136 55 – 650 Asterionella formosad 318 171 46 1.7 645 Aulacoseira binderanac 247–281 137–159 44 – 1 380 Aulacoseira granulatab 519 – – 4–5 847 Fragilaria capucinac 197–215 99–109 50 – 350 Fragilaria crotonensisb 272 – – 2 623 Stephanodiscus sp.c 115–122 62–66 47 – 310 Stephanodiscus hantzschiib 58 – – 0.9 600 Stephanodiscus rotulab 2770 – – 41 5 930 Tabellaria flocculosa 525 279 47 2.5 1 725 v. asterionelloidesb Tabellaria flocculosa v. 383–407 205–210 47 – 820 asterionelloidesc Cryptophytes Cryptomonas ovatab 2090 – – 33 2 710 Dinoflagellates Ceratium hirundinellab 18790 – – 237 43 740

a Data for Planktothrix is per 1 mm length of filament. b From compilation of previously unpublished measurements of field-collected material, as specified in Reynolds (1984a). c From Nalewajko (1966). d From later data of Reynolds (see 1997a). Source: List assembled by Reynolds (1984a) from thitherto unpublished field data, and from data of Nalewajko (1966). THE CONSTRUCTION AND COMPOSITION OF FRESHWATER PHYTOPLANKTON 27 planktic cells will be equivalent to between 0.41 and 0.47 pg µm−3.Infact, the data suggest an order-of-magnitude range, from 0.10 to 1.65 pg 105 µm−3.Inpart, this reveals an inherent danger in the interpretation of a wide spread of raw 104 data through log/log representations. Caution is required in interpolating species-specific deriva- 103 tions from a general statistical relationship. How- ever, the additional difficulty must also be recog- 2

(cell dry / pg) weight 10 nised that the regression is fitted to phytoplank- c tonofconsiderable structural variation (vacuole W space, carbonate or silica impregnation of walls). 10 Accumulated dry mass is also influenced by the physiological state of cells and the environmental conditions obtaining immediately prior to 10 102 103 104 105 the harvesting of the analysed material. It is, v (µm3) perhaps, surprising that the data used to construct Table 1.3 and Fig. 1.8,basedonanalyses Figure 1.8 Log/log plot of cell dry mass (Wc) against cell of material drawn largely from wild populations, volume (v)for various freshwater phytoplankers (data in Table t d should show any consistency at all. Thus, the 3: , Cyanobacteria; , diatoms; , chlorophytes; others). = 0.99 patterns detected are worthy of slightly deeper The equation of the regression is Wc 0.47 v . Redrawn investigation. from Reynolds (1984a). For instance, the variation in the percentage ash content (where known) appears to be considerable. Nalewajko (1966;seealsoTable 1.3)found silicon in lakes and oceans are frequently inad- that ash accounted for between 5.3% and 19.9% equate to meet the potential demands of unfet- (mean 10.2%) of the dry weights of 16 species of tered diatom development. On the other hand, planktic chlorophytes but for between 27% and the requirement is obligate and within relatively 55% (mean 41.4%) of those of 11 silicified diatoms. narrow, species-specific ranges and uptake is subject to physiologically definable levels. The biolog- 1.5.2 Skeletal silica ical availability of silicon, its consumption and Much of the high percentage ash content of the deployment, as well as the fate of its biogenic diatoms is attributable to the extent of silicifi- polymers, are of special relevance to planktic cation of the cell walls. Besides their value to ecology, as they may well determine the envi- taxonomic diagnosis, the ornate and often del- ronmental carrying capacity of new diatom pro- icate exoskeletal structures, celebrated in such duction. Thus, they have some selective value for photographic collections as that of Round et particular types of diatom, or for other types al.(1990), command wonder at the evolution- of non-siliceous plankter, when external supplies ary trait and at the genetic control of frustule are substantially deficient. assembly. There are ecological ramifications, too, The cells of all living organisms have a arising from the relatively high density of the requirement for the small amounts of silicon deposited silicon polymers, seemingly quite oppo- involved in the synthesis of nucleic acids and site to the adaptive requirements for a plank- proteins (generally <0.1% of dry mass: Sullivan tic existence. Moreover, the amounts of silicon and Volcani, 1981). However, it is the demands consumed in the development of each individ- of those groups of protistans and poriferans that ual diatom cell have to be met by uptake of sili- characteristically employ silicon in skeletal struc- con dissolved in the medium. Whatever may have tures – notably diatoms, other chrysophytes radi- been the situation at the time of their evolu- olarians and sponges – that impinge most on tion, the present-day concentrations of dissolved thegeochemical cycling of silicon (Simpson and 28 PHYTOPLANKTON

Volcani, 1981). In passing, it should be noted as fenestration, strengthening ribs, bracing struts that skeletal silica also makes up some 10% of and spines. Later data on some of the species of thedry weight of the grasses, whose co-evolution diatom considered by Einsele and Grim (1938) with the mammals and relative abundance dur- suggest that the area-specific silicon content is ing the tertiary period may have been responsi- particularly responsive to increasing size (see ble for the long-term fluctuations in the export Table 1.5). and availability of the main soluble source of silicon (monosilicic acid: Siever, 1962;Stumm 1.5.3 Organic composition and Morgan, 1996)inthe aquatic environments Discounting the typical 5–12% ash (possibly up to (Falkowski, 2002). 80% in the case of some diatoms) content of air- For the moment, our concern is with the dried plankters, the balancing mass is supposed cell content of silicon. Most is deposited as to be the organic components of the cell, derived acryptocrystalline polymer of silica ((SiO2)n), from the living protoplasm. In comprising mainly resembling opal (Volcani, 1981). The silica con- proteins, lipids and condensed carbohydrates, tents ofseveralspecies of planktic diatoms have albeit in variable proportions, the elemental com- been derived, either by direct analysis or, indi- position of the ash-free dry material is dominated rectly, from the depletion of dissolved silicon by carbon (C), hydrogen (H), oxygen (O) and nitro- byaknownspecific recruitment of cells by gen (N), together with smaller amounts of phos- growth. Unlike other elements critical to their phorus (P) and sulphur (S). At least 14 other ele- survival, diatoms take up scarcely more silicon ments (Ca, Mg, Na, Cl, K, Si, Fe, Mn, Mo, Cu, Co, than is immediately required to form the frus- Zn, B, Va) are consistently recoverable if sufficient tules of the next generation (Paasche, 1980; Sulli- analytical rigour is applied (Lund, 1965). It is van and Volcani, 1981). As already indicated, the impressive that, whilst alive, every planktic cell amounts deposited are generally quite species- had not only the capability of taking up these specific (Reynolds, 1984a;see also Table 1.4), elements from extremely dilute media but also at least when variability in cell size is taken thesuccess in doing so. This should be borne into account (Lund, 1965;Jaworski et al., 1988). in mind when interpreting the relative quanti- Cell-specific silicon requirements differ consid- ties in which these elements occur in the dry erably among planktic species, reportedly rang- matter of cells, because not all were necessar- ing between 0.5% (in the marine Phaeodactylum ily equally available relative to demand. Besides tricornutum:Lewinet al., 1958) and 37% of dry falling deficient in one element that is relatively weight (in some freshwater Aulacoseira spp.: Lund, scarce, others that are relatively abundant may 1965;Sicko-Goad et al., 1984). tend to accumulate in the cell. In this way, the In terms of mass of silicon per cell, broad rela- ratios in which the elements make up the ash- tionships with the mean volume and with the free air-dried algal tissue often give a reliable mean surface area are demonstrable (Fig. 1.9). reflection of the conditions of nutrient availabil- The regressions reflect the increasing silicon ity in the growth medium. Compounded by the deployment with increasing cell size but their special mechanisms that cells may have for tak- slopes, within the interpretative limits of log/log ing up and retaining elements from unreliable relationship, suggest that increased cell size environmental sources (to be explored in Chap- is accompanied by a decreasing ratio of sili- ter 4), the absolute quantities of several of the con : enclosed volume and an increasing ratio of component elements are liable to wide variation. silicon : area. This is in accord with the expecta- Notsurprisingly, the elemental ratios in tion of Einsele and Grim (1938), among the ear- natural phytoplankton plankton have for long liest investigators of the silicon requirements of aroused the interest of physiological ecologists diatoms, that interspecific variations in deploy- and of biogeochemists and they have been ment are related to differences in shape (surface much studied and reported. Absolute quantities area-to-volume effects), together with the rela- do vary substantially, as do the ratios among tive investment in such species-specific features them. Yet, remarkably, the same data indicate THE CONSTRUCTION AND COMPOSITION OF FRESHWATER PHYTOPLANKTON 29

Ta b l e 1.4 The silicon content of some freshwater planktic diatoms

−1 a Species Si (pg cell )Si nSiO2 References (% dry wt) (% dry wt) Asterionella 65.2 (45.5–80.3) – – Einsele and Grim (1938) formosa 64.3 (46.9–82.1) 21 45 Lund (1950, 1965) 61.0 (52.1–69.9) – – Reynolds and Wiseman (1982) 64.3 20 43 Reynolds (1997a), given as Si 0.239W1.003 24 51 Regression of Jaworski et al. (1988) fitted to measurements made on a cultured clone of diminishing size, data given as Si Fragilaria 88.7 (79.8–100.9) – – Einsele and Grim (1938) crotonensis 88.7 (88.2–89.2) 22 46 Lund (1965) 117.8 (98.0–142.7) – – Reynolds and Wiseman (1982) 49.7 (41.3–55.9) – – Reynolds (1973a) Aulacoseira 61.0 – – Einsele and Grim (1938) granulata 291.0 25 54 Prowse and Talling (1958) 138.0 27 57 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake Aulacoseira 111.2 (77.4–128.6) 30 63 Lund (1965) subarctica Stephanodiscus 3989 – – Einsele and Grim (1938) rotula 1942 (1704–2182) – – Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake 1075 – – Gibson et al.(1971) 978 32 69 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake 751 27 58 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake Stephanodiscus 19.2 (15.0–22.1) 26 55 Lund (1965), Swale (1963) hantzschii 16.4 28 60 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake Tabellaria 185.4 ––Einsele and Grim (1938) flocculosa (173.6–197.1) var. 145.5 25 53 Lund (1965) flocculosa (117.3–197.1) a Original citations quote content of SiO2, except where stated otherwise. 30 PHYTOPLANKTON

dry weight (Ketchum and Redfield, 1949). A slightly lower range (45–51%) was derived by Round (1965)andFogg (1975)from measurements on freshwater phytoplankton. However, thesame sources of data showed extremes of about 35%, in cells deprived of light or a supply of inorganic carbon, and 70%, if deficiencies of other elements impeded the opportunities for growth. The importance of carbon assimilation by photoautotrophs to system dynamics has encouraged interest in being able to make direct estimates of organismic carbon content as a function of biovolume. It will be obvious, from the recognition of the variability in the absolute contents of carbon, its proportion of wet or dry biomass, and the relative fractions of ash and vacuolar space, that any general relationship must be subject to a generous margin of error. For instance, Mullin et al.(1966) derived an order-of-magnitude range of 0.012–0.26 pg C µm−3 foraselection of 14 marine phytoplankters that included large and small diatoms. Reynolds’ (1984a) analysis of data, pertaining exclusively to freshwater forms, adopted simultaneous approaches to diatoms Figure 1.9 The silicon content of selected diatoms from and non-diatoms. The relatively low ash content t the freshwater ( )ormarine ( )phytoplankton or other and absence of large vacuoles among the latter aquatic habitat (), plotted on log/log scales against (a) cell permitted a much narrower relationship between volume and (b) surface area. Ast refers to Asterionella, Fra to Fragilaria and Ste to species of Stephanodiscus; Bac refers to carbon and biovolume (averaging 0.21–0.24 pg −3 Bacillaria, Dit to Ditylum, Nit to Nitzschia,SketoSkeletonema C µm ). Supposing carbon makes up a lit- and Tha to Thalassosira. The equations of the least-squares tle under half of the ash-free dry mass and − regression fitted to the data in (a) is log [Si] = 0.707 log v – that dry mass averages 0.47 pg µm 3 (Fig. 1.8), 0.263 (r = 0.85); that for (b) is log [Si] = 1.197 log s – 1.634 this figure is highly plausible. For diatoms, (r = 0.83). Redrawn, with permission, from Reynolds (1986a). there seemed little alternative but to calculate carbon as a function of the silica-free dry mass. This approach does not satisfy the quest for collectively that the quantities of the compo- avolume-to-carbon conversion for mixed diatom- nents vary within generally consistent limits and, dominated assemblages, which continues to tax though they do fluctuate, the ratios with other ecosystem ecologists. A recent re-exploration by constituents do not vary by more than can be Gosselain et al.(2000) confirms the wisdom of sep- reasonably explained in these terms. arating diatoms from other plankters. It provides For instance, carbon generally makes up an evaluation of several of the available formu- about half the dry organic mass of organic cells. laic methods for estimating the carbon contents The normal content of phytoplankton strains of various diatoms. cultured under ideal laboratory conditions of Of the other elements comprising biomass, constant saturating illumination, constant tem- nitrogen accounts for some 4–9% of the ash-free perature and an adequate supply of all nutri- dry mass of freshwater phytoplankters, depend- ents, was found to be 51–56% of the ash-free ing on growth conditions (Ketchum and Redfield, THE CONSTRUCTION AND COMPOSITION OF FRESHWATER PHYTOPLANKTON 31

Ta b l e 1.5 The silicon content of some planktic diatoms relative to cell volume and surface area

Species Si v s Si Si Referencesa (pg cell−1) (µm3) (µm2) (pg µm−3) (pg µm−2) Asterionella 61.0 630 860 0.097 0.071 Reynolds and Wiseman formosa (1982) Fragilaria 117.8 780 1080 0.151 0.109 Reynolds and Wiseman crotonensis (1982) Stephanodiscus 1075 8600 2574 0.125 0.418 Gibson et al.(1971) rotula 1942 15980 4390 0.122 0.442 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake 978 8300 2580 0.118 0.379 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake 751 5930 1980 0.127 0.379 Thitherto unpublished records cited in Reynolds (1984a), calculated indirectly from SiO2 uptake Stephanodiscus 16.4 600 404 0.027 0.041 Thitherto unpublished records hantzschii cited in Reynolds (1984a), calculated indirectly from SiO2 uptake

a All citations converted from the original published data quoted content in terms of SiO2,by multiplying by 0.4693.

1949;Lund, 1965, 1970;Round, 1965). Maxi- range 0.2–0.4% of ash-free dry mass. The inves- mum growth rates are sustained by cells con- tigation of Mackereth (1953)ofthe phosphorus taining nitrogen equivalent to some 7–8.5% of contents of the diatom Asterionella formosa, which ash-free dry mass. Among freshwater algae, at reported a range of 0.06 to 1.42 pg P per cell, is least, the phosphorus content is yet more vari- much cited to illustrate how low the cell quota able, although again, maximum growth rate is may fall. The lower value, which is, incidentally, attained in cells containing phosphorus equiva- corroborated by data in earlier works (Rodhe, lent to around 1–1.2% of ash-free dry mass (Lund, 1948;Lund, 1950), corresponds to ∼0.03% of ash- 1965;Round, 1965). Growth is undoubtedly pos- free dry mass. On the other hand, cell phos- sible at rather lower cell concentrations than phorus quotas may be considerably higher than this but further cell divisions cannot be sus- theminimum (certainly up to 3% of ash-free tained when the internal phosphorus content is dry mass is possible: Reynolds, 1992a), especially toosmall to divide among daughters and can- when uptake rates exceed those of deployment not be replaced by uptake. This concept of a mini- and cells retain more than their immediate needs mum cell quota (Droop, 1973) has been much used (so-called luxury uptake). Uptake and retention of in the understanding the dynamics of nutrient phosphorus when carbon or nitrogen supplies limitation and algal growth: for phytoplankton, are limiting uptake (cell C or N quotas low) may the threshold minimum seems to fall within the also result in high quotas of cell phosphorus. 32 PHYTOPLANKTON

Analogous arguments apply to the minimal therecommendation. The fourth line relates the quota of all the other cell components. How- Redfield ratio to the base of carbon (= 100, for ever, itisthevariability in the carbon, nitrogen convenience), while further entries give elemen- and phosphorus contents that is most used by tal ratios for specific algae, reported in the litera- plankton ecologists to determine the physiologi- ture but cast relative to carbon. Chlorella is a fresh- cal state of phytoplankton. Taking the ideal quo- water chlorophyte and Asterionella (formosa)isa tas relative to the ash-free dry mass of healthy, freshwater diatom, having a siliceous frustule. growing cells as being 50% carbon, 8.5% nitro- The ‘peridinians’ are marine. Approximations of genand 1.2% phosphorus, these elements occur theorder of typical elemental concentrations in in the approximate mutual relation 41C : 7N : 1P lake water are included for reference. They are (note, C : N ∼6). Division by the respective atomic sufficiently coarse to pass as being applicable to weights of the elements (∼12, 14, 31) and normal- the seas aswell.The important point is that ising to phosphorus yields a defining molecular plankters are faced with the problem of gath- ratio for healthy biomass, 106C : 16 N : 1P. ering some of these essential components from This ratio set iswellknownandisgenerally extremely dilute and often vulnerable sources. referred to as the Redfield ratio.Asayoung marine As applied to phytoplankton, the Redfield scientist, A. C. Redfield had noted that the com- ratio is not diagnostic but an approximation position of particulate matter in the sea was sta- toanormal ideal. However, departures are real ble and uniform in a statistical sense (Redfield, enough and they give a strong indication that the 1934)and,ashelatermadeclear,‘reflected... cell is deficient in one of the three components. the chemistry of the water from which materials Extreme molecular ratios of 1300 C : P and 115 are withdrawn and to which they are returned’ N:P in cells of the marine haptophyte, Pavlova (Redfield, 1958). The notion of a constant chem- lutheri, cultured to phosphorus exhaustion, and ical condition was clearly intended to apply on of 35 C : P and 5 N : P in nitrogen-deficient strains ageochemical scale but the less-quoted investi- of the chlorophyte Dunaliella (from Goldman et al., gations of Fleming (1940)andCorner and Davies 1979), illustrate the range and sensitivity of the (1971) confirm the generality of the ratio to living C :N:Prelationship to nutrient limitation. plankton. Because the normal (Redfield) ratio is indica- It is, of course, very close to the approxi- tive of the health and vigour that underpin rapid mate ratio in which the same elements occur cell growth and replication, and given that depar- in the protoplasm of growing bacteria, higher tures from the normal ratio result from the plants and animals (Margalef, 1997). Stumm and exacting conditions of specific nutrient deficien- Morgan (1981;seealso1996)extended the ideal cies, it is tempting to suppose that cells to which stoichiometric representation of protoplasmic thenormal ratios apply are not so constrained composition to the other major components and must therefore be growing rapidly (Goldman, (those comprising >1% of ash-free dry mass – 1980). It would follow that, given the stability hydrogen, oxygen and sulphur) or some of those of the ratio in the sea, natural populations hav- that frequently limit phytoplankton growth in ing close-to-Redfield composition are not only not nature (silicon, iron). The top row of Table 1.6 nutrient-limited but may be growing at maximal shows the information by atoms and the sec- rates. This may be sometimes true but there is ond by mass, both relative to P. The third line is apossibility that biomass production in oceanic recalculated from the second but related to sul- phytoplankton is less constrained by N or P than phur. Unlike carbon, nitrogen or phosphorus, sul- wasonce thought (see Chapter 4). However, there phur is usually superabundant relative to phyto- are other constraints on growth rate and upon plankton requirements and plankters have no nutrient assimilation into new biomass, which special sulphur-storage facility. Following Cuhel may tend to uncouple growth rate from nutrient and Lean (1987a, b), sulphur is a far more stable uptake rate (see Chapter 5). Tett et al.(1985)pro- base reference and deserving of wider use than it vided examples – of phytoplankton in continuous receives. Unfortunately, few studies have adopted culture, of natural populations of Cyanobacteria THE CONSTRUCTION AND COMPOSITION OF FRESHWATER PHYTOPLANKTON 33

Ta b l e 1.6 Ideal chemical composition of phytoplankton tissue and relative abundance of major components by mass

CHONPSSi Fe References Redfield atomic ratio 106 263 110 16 1 0.7 trace 0.05 Stumm and Morgan (atomic (1981) stoichiometry rel to P) Redfield ratio by mass 41 8.5 57 7 1 0.7 trace 0.1 Stumm and Morgan (stoichiometry rel (1981) to P) Redfield ratio by mass 60 12 81 10 1.4 1 Stumm and Morgan (stoichiometry rel (1981) to S) Redfield ratio by mass 100 16.6 2.4 Stumm and Morgan (stoichiometry rel (1981) to C) Chlorella 100 15 2.5 1.6 trace Round (1965) (dry weight rel to C) Peridinians 100 13.8 1.7 6.6 3.4 Sverdrup et al.(1942) (dry weight rel to C) Asterionella 100 14 1.7 76 Lund (1965) (dry weight rel to C) Medium (mol L−1)10−3 102 102 10−4 10−6 10−3 10−2 <10−5 Author’s approximation but omitting dissolved nitrogen gas

stratified deep in the light gradient, and of spring distribution among all the photoautotrophic blooms of the diatom Skeletonema costatum in a algae and cyanobacteria, the photosynthetic pig- Scottish sea loch – where growth rates were kept ment chlorophyll a is also widely used as a con- very low but the cell contents of carbon, nitro- venient index of phytoplankton biomass. This gen and phosphorus stayed close to the Red- makes its contribution to cellular composition field ideal in each instance. It is even possible extremely important to extrapolating to phyto- that natural cells do not drift as far from the plankton abundance and to its use as a base for ideal as it possible to force them under labora- estimating phytoplankton productivity. Although tory conditions. How cells balance availability, there have been many values published alluding uptake, storage and self-replication over the to the absolute chlorophyll a contents of freshwa- period of a single generation will be explored in terphytoplankton (some reviewed in Reynolds, Chapter 4. 1984a), these quantities are now known to be so variable that they have little value by them- 1.5.4 Chlorophyll content selves. The variability is most obviously linked to Besides being a distinguishing constituent the cell’s requirement for carbon and the light of phytoplankton and having a universal energy available to drive its fixation. In broad 34 PHYTOPLANKTON

dry weight) between its deep-stratiﬁed and free- 1000 mixed phases (Reynolds 1997a). On the other hand and analogously with Redﬁeld stoichiometry, the probabilistic relation- 100 ships derived from mixed populations over periods of time point to 0.003–0.007 pg µm−3,or roughly 0.013–0.031 pg chl (pg cell C)−1,or

10 0.7–1.6% of the ash-free dry mass as each being content / pg a typical. For many purposes, the common approximations that chlorophyll accounts for 1% of the dry mass and about 2% of the value of the cell 1 carbon quota are not at all unreasonable average estimates. Indeed, field chlorophyll measure- Cell chlorophyll Cell chlorophyll 3 ments are commonly converted to approximate 0.1 producer biomass, expressed as active cell carbon 1 by the application of a ratio 50 : 1 by weight. A 4 margin of variation, from 30 : 1 to 70 : 1, should 2 nevertheless be allowed. It should be borne in 0 10 102 103 104 105 Cell volume (µm3) mind too that the amount of chlorophyll a is proportionate to cell volume and not cell num- Figure 1.10 Log/log plot of cell chlorophyll-a content ber, bigger cells carrying proportionately more against cell volume of various freshwater phytoplankters (data chlorophyll than small ones, and that there may in Table 1.3): t, Cyanobacteria; d, diatoms; , chlorophytes; be systematic interphyletic differences in the typ- , others). Regression equations are fitted to the data for ical cell-specific contents. The plot of data taken Cyanobacteria (1, log chl = 1.00 log v – 2.26), diatoms (2, log from Reynolds (1984a)emphasises both points = = chl 1.45 log v – 3.77) and chlorophytes (3, log chl 0.88 (Fig. 1.10). log v – 1.51) and to all points (4, log chl = 0.98 log v – 2.07). Redrawn from Reynolds (1984a).

terms, the weaker is the photon flux, and the 1.6 Marine phytoplankton greater istheprobability of limitation of growth rate by light, then the greater is the need for The information on the size, morphology and ele- thelight-harvesting centres of which the chloro- mental composition of phytoplankton presented phyll is an essential component. Where appropri- in this chapter has been dominated by relation- ate, this behaviour may be accompanied by the ships detected among freshwater species. This is production of additional quotas of accessory pig- partly attributable to the interests and experiments (for a fuller discussion, see Chapter 3). Syn- ences of the author and not to any lack of cor- thesis of chlorophyll a is also sensitive to nutri- responding data for the sea; useful data compila- ent supply and deployment, directly or as a con- tions are to be found in, for instance, Mullin et sequence of altered internal resource allocation. al.(1966), Strathmann (1967), Sournia (1978)and The measurements of biomass-specific estimates Verity et al.(1992). However, it seemed more inter- of chlorophyll a presented in Reynolds (1984a) esting to take the data and derivations of Mon- range over an order of magnitude, between tagnes et al.(1994), corrected for live cell volumes 0.0015 and 0.0197 pg µm−3 of live cell volume, as opposed to those of material shrunk by preser- which corresponds to 3 to 39 mg g−1 of dry mass vatives, and to compare their findings with the (0.3% to 3.9%). The true range is probably wider: patterns presently discerned among freshwater later data showed that the chlorophyll-a content species. of just one species of cyanobacterium, Planktothrix Montagnes et al.(1994) compiled a thorough cf. mougeotii,may vary nearly ninefold (0.45–3.9% compilation of the dimensions and volumes of MARINE PHYTOPLANKTON 35

Ta b l e 1.7 Some cell measurements of cultured marine phytoplankton

Species shapea MLD v CNChla (µm) (µm3) (pg cell−1) (pg cell−1) Prasinophytes Micromonas pusilla ps 2 2 0.8 0.1 0.01 Mantoniella squamata sph 4 25 3.6 0.6 0.15 Chlorophytes Nannochloris ocelata sph 3 4 1.4 0.2 0.05 Dunaliella tertiolecta sph 8 201 41.7 7.9 1.8 Chlamydomonas sp. sph 19 3 300 969.7 129.6 11.3 Diatoms Thalassiosira pseudonana cyl 4 20 5.9 0.94 0.2 Thalassiosira weissﬂogii syl 19 286 64.4 11.1 1.5 Detonula pumila cyl 36 4 697 355.2 61.4 7.4 Chrysophytes Pelagococcus sp. sph 5 18 2.8 0.7 0.1 Pseudopedinella pyriformis ps 9 80 18.0 2.9 0.7 Apedinella spinifera sph 10 222 47.6 9.9 2.3 Haptophytes Emiliana huxleyi sph 5 25 4.6 1.0 0.1 Pavlova lutheri ps 6 25 8.5 1.2 0.2 Isochrysis galbana sph 6 38 7.0 1.2 0.2 Phaeocystis pouchetii ps 6 45 5.5 1.3 0.1 Chrysochromulina herdlensis sph 7 74 8.2 1.9 0.2 Prymnesium parvum ps 8 79 15.1 2.0 0.3 Coccolithus pelagicus sph 12 620 65.5 14.5 1.9 Cryptophytes Rhodomonas lens ps 10 203 40.7 11.4 0.7 Chroomonas salina ps 11 167 32.4 7.9 0.9 Pyrenomonas salina ps 12 181 32.4 7.0 1.4 Cryptomonas profunda ps 17 765 104.7 21.0 2.6 Dinophytes Gymnodinium simplex ps 11 224 38.0 8.3 0.7 Gymnodinium vitiligo ps 14 683 113.8 22.6 2.3 Gyrodinium uncatenatum ps 32 11 246 2275.3 441.0 37.3 Gymnodinium sanguineum ps 56 31 761 2913.2 688.4 57.4 Karenia mikimotoi ps 24 3 399 513.9 93.8 12.9 Raphidophytes Heterosigma carterae ps 16 362 87.8 17.7 3.8 a Shapes: cyl, cylindrical; ps, prolate spheroid; sph, spherical. Source: After Montagnes et al.(1994). 36 PHYTOPLANKTON

and a statistically predictable pattern of the relative quantities of the various constituents. This simple fact contributes to the fascination for students of phytoplankton ecology as the subject embraces the observable wonder of the seasonal replacement of one dominant among many species by another among others, as well as the opportunity to express the dynamics of production and attrition and of population wax and wane in empirical terms interlinked by powerful and predictable statistical relationships. The scene is set for the subsequent chapters.

1.7 Summary

The chapter provides an introduction to phytoplankton. The phytoplankton is defined as a collective of photosynthetic microorganisms, adapted to live partly or continuously in the open Figure 1.11 Log/log relationships between (a) cell carbon, of the seas, of lakes (including reservoirs), ponds (b) cell nitrogen and (c) chlorophyll-a content and cell volume and river waters, where they contribute part or in the marine phytoplankters listed in Table 1.7. Redrawn, most of the organic carbon available to pelagic with permission, from Montagnes et al.(1994). food webs. Although their taxonomy is currently undergoing major revision and even the phylo- 30 or so species of phytoplankton, representative genies are questioned, it is difficult to be cat- of various phyla and covering a good range of egorical about the species representation and cell sizes, together with measured cell quotas of phyletic make-up of phytoplankton. It is reason- carbon, nitrogen, protein and chlorophyll a. The able to point to the description of some 4000 to material reproduced in Table 1.7 represents but a 5000 species from the sea and, probably, a similar fragment of the original. Live cell volumes cover order of species from inland waters. The species asimilar series of magnitudes as the freshwa- belong to what appear to be 14 legitimate phyla, ter species listedinTable1.2. The carbon content coming from both bacterial and eukaryotic pro- of cells varied between 0.08 and 0.4 pg µm−3, tist domains. In both the marine and the fresh- with a mean value of 0.20. The ratio of carbon- waterphytoplankton, there is a wide diversity of to-nitrogen varied between 3.6 and 7.6 by mass, size, morphology, colony formation. Though gen- with a mean of 5.43. Chlorophyll a fell within the erally microscopic, phytoplankton covers a range range 0.001–0.009 pg µm−3. of organism sizes comparable to that spanning Some log/log relationships from the work forest trees and the herbs that grow at their of Montagnes et al.(1994)areplotted in Fig. bases. 1.11.Carbon,nitrogen and chlorophyll are each The early history of phytoplankton studies closely correlated to live cell volume and in a is recapped. Although a knowledge of some of way which is similar to the corresponding rela- theorganisms goes back to the invention of the tionships among the freshwater phytoplankton. microscope, and many genera were well known Thus (and, again, as is true for the freshwater to nineteenth-century microscopists, their role phytoplankton), despite a remarkable diversity in supporting the aquatic food webs of open of phylogeny and morphology, as well as a 5- water, culminating in commercially exploitable orders-of-magnitude range of cell volumes, there fish populations, was not realised until the 1870s. is an equally striking pattern of cell composition The early work by Muller,¨ Haeckel and Hensen SUMMARY 37

(who invented the name ‘plankton’) is brieﬂy mineral-reinforced walls, carbon accounts for described. Some of the terms used in plankton about 50% of the dry mass, nitrogen about 8–9% science are noted with their meanings, while and phophorus between 1% and 1.5%. Relative to those that appear still to be conceptually useful phosphorus, these amounts correspond to a prob- are singled out for retention. abilistic atomic ratio of 106 C : 16 N : 1 P, close to Despite variation of several orders of magni- theso-called Redﬁeld ratio for particulate matter tude in the sizes of plankters, there is a pow- in the ocean. It is also similar to the composi- erful trend towards conservatism of the surface- tion of most living protoplasm. The amounts are to-volume ratio, which is achieved through dis- related also to hydrogen, oxygen, silicon, sulphur tortion and departure from the spherical form and iron. Up to 12 other elements are regularly among the larger species. This aids exchange of present in phytoplankton in trace proportions. gases, nutrients and other solutes across the cell Departures from the ratio are rarely systematic, surface and it also has some role in prolongation merely indicative of one of the highly variable of suspension. In an apparently diametrically components falling to the minimum cell quota. opposite trend, some algae form mucilaginous The amount of chlorophyll a is also highly coenobia that have very low surface-to-volume variable according to growth conditions but nev- ratios. When it is combined with some other ertheless tends to average about 1% of the ash- power of motility, the streamlining effect allows free dry mass of the cell and to represent about the colony to move relatively quickly through 2% of the elemental carbon. A carbon:chlorophyll water and to move to a more favourable position value of 50 : 1 is considered typical but it may in the water column. vary routinely between about 70 : 1 (cells in high The construction and composition of plank- light) to 30 : 1 or lower (in cells exposed to con- ton are critically reviewed. Apart from a vari- sistently low light). ety of scales, exoskeleta, plastid type and pig- Despite the extreme diversity of phylogeny, ment composition, the ultrastructural compo- morphology and size, both the marine and the nents and architecture of the living protoplasm freshwater phytoplankton are characterised by a are comparable among the phytoplankton. Sim- striking and statistically predictable blend of ele- ilarly, the elemental make-up of the protoplast mental constituents. This proves very helpful in is similar among all groups of phytoplankton, quantifying production and attrition processes ideally occurring in approximately stable rela- contributing to the dynamics of natural, func- tive proportions. Discounting the ash from the tioning assemblages of plankton. Chapter 2

Entrainment and distribution in the pelagic

thepersistence of the clone that residence is con- 2.1 Introduction tinuous, only that individuals of any given generation spend sufficient of their life in the photic The aims of this chapter are to develop an appre- zone to make the net autotrophic gains in syn- ciation of the adaptive requirements of phyto- thesised carbon, over the burden of respiration, plankton for pelagic life and to demonstrate the to be able to sustain the next cell replication. The consequences of its embedding in the movements point here is that the essential adaptation is to of the suspending water mass. The exploration maximise the exposure to adequate light, by any begins by dismissing the simplistic notion that appropriate mechanism. the essential requirement of plankton is to pre- The mechanisms for this are not self-evident, vent or minimise the rate of sinking, in the sense unless the behaviour of the water itself is taken that this will prolong its residence in the upper into account. For this is the feature that the clas- part of the water column. This would be a clear sical explanation of phytoplankton adaptations nonsense, were there no counteractive mecha- rather omits – that, at every scale, the water is nism to ensure that organisms start out at the never a passive component. Under the influence topofthe water in the first instance. Moreover, of its warming and cooling, of the influence of slow sinking from the upper layers is of illusory gravity, the pull of the Moon, of the work of wind respite if the downward passage to depths beyond and even of the rotation of the Earth, water is in the adequacy of penetrating light, whether that motion. Some of these inputs are continuously is 50 cm or 50 m beneath the water surface, variable, and their various interactions with the is inevitable, unless there is some mechanism internal viscous forces contribute to a spectrum for the organism’s return. Manifestly, it is not of motion that is characteristically variable, in enough just to reduce the rate of irreversible sink- both time and space. ing to qualify as a phytoplankter. Thus, there is an explicit, inescapable and Prolonged residence in the upper insolated variable velocity component to the medium. layers of the open water of lakes and seas (the Moreover, the movement is, almost always, turbu- photic zone) is, without doubt, a primary require- lent, so that flow tends to be in billowing eddies ment of the individual phytoplankter, ifitisto rather than along direct trajectories. Such move- synthesise sufficient organic carbon to build the ments are capable of alternately enhancing or tissue of the next generation. The survival of the counteracting the intrinsic velocity of the verti- genetic stock and the seed population capable cal tendency of the settling plankter and, within of providing the base of subsequent generations thefinite bounds of the water mass, may force may also depend upon the survival of a rela- its lateral displacement or even push it upwards. tively small number of extant individuals. It is These possibilities are the basis of the not a condition either for the individual or for principle of entrainment of phytoplankton in MOTION IN AQUATIC ENVIRONMENTS 39

Ta b l e 2.1 Comparison of the physical properties of air, pure water and sea water

Air Pure water Sea water

−3 3 3 Maximum density, ρw (kg m ) 1.2 1 × 10 ∼1.03 × 10 Absolute viscosity, η (kg m−1 s−1) 1.8 × 10−5 1 × 10−3 ∼1.1 × 10−3 themotion of natural water bodies. Empirical shared between lakes, rivers and the atmosphere, description of entrainment relies on the anal- is less than 0.02%. However, even this fraction, ogous relativity between the intrinsic sinking totalling c. 225 000 km3,isoverwhelmingly dom- velocity of the plankter (ws)andtheturbulent inated by the volume of standing inland waters: velocity of the motion (u∗) This immediately the13largest lakes in the world (by volume) introduces an anomaly, which must be addressed alone hold 160 000 km3 (Herdendorf, 1990). At at once. The idea is that the smaller is ws relative any moment of time, most of this volume is actu- to u∗ then the more complete is the entrainment ally so inhospitable to primary producers that it of the particle in the motion. This is another way is not conducive to phytoplankton development of saying that the best way to ensure entrain- but, because it is fluid and in persistent motion, ment is to minimise the rate of sinking. Isn’t all the volume is potentially available, sooner or this just the idea that was so summarily dis- later. The global rate of the hydrological renewal, missed in the first paragraph? No, for the com- in the cycle of precipitation, flow and evapora- ment was directed to the redundant, notional tion, results in an estimated annual loss from context of a slow settlement of plankters through the ocean of 353 000 km3,made good by direct astatic water column. What is really needed, if precipitation (roughly, 324 000 km3)andnet river full entrainment is the goal, is a slow rate of set- run-off from the land masses (∼29 000 km3). The tlement relative to the water immediately adja- theoretical replacement time for the ocean is cent to the organism and its instantaneous tra- thus around 3800 years. jectory and velocity. The approach adopted in developing this chapter is to first consider the nature, scale and 2.2.1 Physical properties of water How this vast and enduring body of water reacts variability of water movements and the estima- ∗ to theforces placed upon it is related to the some- tion of u .Then the question of settling veloci- what anomalous physical properties of water ties, buoyant velocities and swimming rates (ws) itself. Given its low molecular weight (18 dal- is reviewed, before the consequences on spa- tons), water is a relatively dense, viscous and tial and temporal distributions are considered at barely compressible fluid (see Table 2.1 for ref- the end. erence), with relatively high melting and boiling points. This behaviour is due to the asymmetry of the water molecule and to the fact that the 2.2 Motion in aquatic environments two hydrogen atoms, each sharing its electron with the oxygen atom, are held at a relatively nar- The aquatic environment is the greatest habitat row angle on one side of the molecule. In turn, to be continuously exploited by organisms. Liquid this gives a polarity to the molecule, one side water presently covers about 71% of planet Earth, (the ‘hydrogen side’) having a net positive charge thesea alone occupying 361.3 × 106 km2 of it. The and the other (the ‘oxygen side’) a net negative estimated volume of the sea (∼1 350 000 000 km3) one. The molecules then have a mutual attrac- accounts for 97.4% of all the water on the planet. tion, giving rise to the formation of aquo poly- Taking off the volume stored in the polar ice mers.Itisthe complexation into larger molecules caps (27.8 × 106 km3)andtheamountstored which raises the melting point of what is oth- in the ground (∼8 × 106 km3), the balance, erwise a low-molecular-weight compound into 40 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Figure 2.1 Plots showing (a) the density and (b) the absolute viscosity of pure water as a function of temperature. Redrawn, with permission, from Reynolds (1997a).

the range we perceive as being normal. As tem- opposite-charged poles of the water molecules perature is raised and the motion of molecules all contribute further modifications to the poly- is increased, individual molecules break from merisation. Individual ions become surrounded the complexes. In most liquids, the molecules by water molecules in a hydrated layer, disrupt- come to occupy more space, that is the liquid ing their structure and altering the properties of expands and the density decreases. In water, this the liquid. The salinity of sea water ranges from effect is countered by the fact that the liberated atrace (in some estuaries and adjacent to melt- molecules fall within the complexes, so that the ing glaciers) to a maximum of about 40 g kg−1 same number of molecules occupies less space, (the Red Sea; note that this is greatly exceeded leading to increased density. In pure water, the latin some inland lakes). In most of the open ocean, tereffect dominates up to 3.98 ◦C; above this tem- salinity is generally about 35 (±3) g kg−1,having perature, the separation of molecules becomes, adensity of 27 (±2) kg m−3 greater than pure progressively, the dominant effect and the liquid waterofthe same temperature. The presence of expands accordingly (see Fig. 2.1). salt depresses not just the freezing point but also The molecular behaviour explains not only thetemperature of maximum density. When the why fresh water achieves its greatest density at salt content is about 25 g kg−1,thesetempera- close to 4 ◦Cbutalso why, under appropriate con- tures coincide, at −1.3 ◦C. Thus, in most of the ditions, ice forms at the surface of a lake (where, sea, the density of water increases with lowering incidentally, it insulates the deeper water against temperatures right down to freezing. Sea ice does further heat loss to the atmosphere), and why, not form at the surface, as does lake ice, simply as with every degreestepabove4◦C, the difference a consequence of cooling of the water. Normally, in density also becomes greater. Limnologists are some other component (dilution by rain and or well aware oftheeffect this has in enhancing the terrestrial run-off) is necessary to decrease the mechanical-energy requirement to mix increas- density of the topmost water. ingly warmed surface waters with the dense lay- Molecular behaviour influences the ers below; the limnetic ecologist is familiar with temperature-dependent viscous properties of the impact of both processes on the environ- water. Viscosity, manifest as the resistance ments of phytoplankton. provided to one water layer to the slippage of The same principles apply in the sea and in another across it, decreases rapidly with rising salt lakes, except that the higher concentrations temperature (Fig. 2.1b); according to the stan- of dissolved ionic salts, their separation into con- dard definition of viscosity, this means there is stituent charged ions and their attraction to the adecreasing resistance of one water layer to the MOTION IN AQUATIC ENVIRONMENTS 41 slippage of another across it, for the same given difference in temperature. Viscosity is greater in sea water than in pure water: an increment about 0.1 × 10−3 kg m−1 s−1 applies to water containing 35 g kg−1 over a normal temperature range. High viscosity, like large differences in density, is an effective deterrent to physical mixing and mechanical heat transfer.

2.2.2 Generating oceanic circulation It is also relevant to the generation of major flows that water has a high specific heat, which in essence means that it takes a lot of heating to raise its temperature (4186 J to raise 1 kg by 1 ◦C, or by 1 kelvin).However,itisjustasslowto lose it again, save that evaporation, turning water liquid into vapour, is very consumptive of accumulated heat (2.243 × 106 Jkg−1). Nevertheless, theexchange of incoming and outgoing heat is amajorcomponent in the physical behaviour of the oceans. In fact, the patterns of motion are subject to a complex of drivers and the outcome is usually complicated. Empirical description of motion can only be probabilistic and, in any case, far beyondthescope of this book. In essence, the Figure 2.2 (a) The spectrum of the solar flux at ground energy to drive the circulation comes from the level compared to that of the ‘solar constant’ at the top of Sun. Because of its relevance also to local vari- the atmosphere; the visible wavelengths (light) are shown ability in heat exchanges and its obvious links hatched. (b) Daily integrals of undepleted solar radiation at to the energy fluxes used in photosynthesis, a the top of the atmosphere, shown as a function of latitude deeper consideration is given later to the solar (degrees) and time of year in the northern hemisphere. The irradiance fluxes. For the moment, it is necessary approximate match for the southern hemisphere is gained by to accept that the proportion of the solar energy displacing the horizontal scale by 6 months. Redrawn, with flux that penetrates the atmosphere to heat the permission, from Reynolds (1997a). surface of the sea or lake is first a function of the solar constant. This is the energy income to a diminishes with latitude and not even the com- notional surface held perpendicular to the solar bination of the tilt of the Earth’s axis and its electromagnetic flux, before there is any reflec- annual excursion round the sun even this out. tion, absorption or consumption in the Earth’s The plots in Fig. 2.2bshow the annual varia- atmosphere. Confusingly, it is not constant, as tion in the undepleted daily flux at each of the the elliptical orbit of the Earth around the Sun selected northern-hemisphere latitudes. varies around the mean distance (149.6 × 106 km) Although the highest potential daily heat flux fluctuates during the year within ±2.5 × 106 km. is everywhere quite similar, sustained heating Besides, the heat radiated from the Sun also fluc- through the year is always likely to be greatest tuates. Nevertheless, there is a valuable reference in the tropics but never for such long diurnal (∼1.36 kW m−2)againstwhich the absorption, periods as occur at high latitudes in summer. reflection and backscatter by dust, water vapour On a rotating but homogeneously water-covered and other gases and, especially, clouds can be Earth having a continuously clear atmosphere, scaled. Even before those losses are deducted (see there would be considerable latitudinal differ- Fig. 2.2a), however, the heat flux per unit area ences in the heat flux directed to the surface 42 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

(other things being equal, sufficient at the equa- atmosphere; its movements are subject to analo- tortoraise the temperature of the top metre by gous global-scale forces. It is its much lower mass, ∼1 ◦Cevery daylight hour, for 12 months of the density and viscosity that gives the impression year). Ignoring night-time losses and any convec- of a different behaviour. In fact, there is close tional heat penetration, the expectation is that coupling between them, in the sense that strong the now less dense surface water, heated in the winds generate waves, drive surface drift cur- tropics, would spread out to the higher latitudes, rents and force the transfer of some of mechan- at least until it had cooled to the temperature of ical energy to the water column. At the same thehigh-latitude water. In compensation, water time, differences in inertia and in specific heat must be drawn from the higher latitudes, via bring differential rates of warming over land adeeperreturnflow.Inthisway,wemayvisu- and water, leading to differences in air pres- alise the initiation of a convectional circulation sure and the superimposition of prevalent wind of hemispheric proportions. conditions. This simplified conception is complicated by The predictability of wind action on individ- several interacting factors. The rotation of the ual water bodies is generally difficult (as are most Earth causes everything on it, including oceanic aspects of weather forecasting), save in probabilis- drift currents, to move eastwards. As surface tic terms, based on the statistics of experience water moves poleward, however, the rotational and pattern recognition. However, the linkage speed of the ground under it lessens and the iner- between wind effects and the motion of water tia of the trajectory tends to pull it ahead of the in which phytoplankton is resident has been solid surface, the relative motion thus drifting deeply explored. Broad flow patterns of surface further east. This easterly deflection, known as currents in the oceans have been discerned and Coriolis’ effect, acts like a laterally applied force. described by mariners over a period of centuries The positions of the continental land masses, of and since committed to oceanographers’ maps course, obstruct the free development of these (for an overview, see Fig. 2.3). Patterns of circu- motions while the irregularity of their distribu- lation in certain large lakes have been described tion gives rise to compensatory latitudinal flows over a rather shorter period of time (e.g. Mor- among the major oceans (especially in the south- timer, 1974;Csanady, 1978)andthose of many ern hemisphere). The variable depth of the ocean smaller lakes have been added in recent years; floor also interferes with the passage of deep the example in Fig. 2.4 is just one such instance. return currents which, locally, may be forced to deflect upwards and to ‘short-circuit’ the potential hemispheric circulation. 2.3 Turbulence Also superimposed upon the circulatory pattern are the tidal cycles exerted by the variable 2.3.1 Generation of turbulence gravitational pull on the water exerted by the Despite the rather self-evident relationship that rotation of the Moon around the Earth, hav- plankton mostly goes where the water takes it, ing frequencies of ∼25 hours and ∼28 days. The thelarge-scale motion of water bodies tells us effect of tides on the pattern of circulation may frustratingly little about what the conditions of not be large in the open ocean but may dom- life are like at the spatial scales appropriate to inate inshore circulations near blocking land- individual species of phytoplankton (generally forms that may trap tidal surges (the Bay of <2mm),oraboutthetrajectories followed by the Fundy, between Nova Scotia and New Brunswick, individual phytoplankter whose survival depends experiences the greatest tidal extremes in the on its passing a reasonable fraction of its life world – over 13 m–andsomeofthe most aggres- in the insolated upper reaches of the water col- sive tidal mixing). umn. Although it has long been appreciated that Surface currents, especially in lakes, are prox- the energy of the major circulations is dissipated imally influenced by wind. Wind is the motion through cascades of smaller and smaller gyra- of air in the adjacent fluid environment, the tory structures, now called the Kolmogorov eddy Figure 2.3 The currents at the surface of the world’s oceans in the northern winter. Redrawn, with permission, from Harvey (1976). 44 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

of turbulence have gradually given way to a developing turbulence theory (Levich, 1962;Ten- nekes and Lumley, 1972) but it is the remarkable progress in instrumentation and direct sensing of turbulence (see especially Imberger, 1998), together with the rapid assimilation of its quantification into physical oceanography and limnology (see, for example, Denman and Gargett, 1983; Spigel and Imberger, 1987;Imberger and Ivey, 1991; Mann and Lazier, 1991; Imboden and Wuest,¨ 1995;Wuest¨ and Lorke, 2003)that have given most to the characterisation of the environment of the phytoplankton. A helpful starting point is to envisage a completely static column of water (Fig. 2.5a). If its upper surface is subjected to a mild horizontal force, τ,then water molecules at the air–water interface are dragged across the surface in the direction of the force. Their movement is transmitted to the layer below, which also begins to move, albeit at a lesser velocity. Further downward propagation soon leads to a configuration envisaged in Fig. 2.5b, each layer of molecules sliding smoothly over the one below, in what is described as laminar flow. The structure con- formstoavertical gradient of horizontal velocities, u,thesteepness of which is defined by the Figure 2.4 Model reconstructions of the near-surface / currents generated in Esthwaite Water, UK, by steady winds differential notation, du dz (literally the incre- of 5 m s−1 and various orientations. The longest axis of the ment or decrement of horizontal velocity for lake is approximately 2.2 km. Redrawn, with permission, from asmall increment in the vertical direction, z). Falconer et al.(1991). While the condition of laminar flow persists, the ratio between the applied force (per unit area) and the velocity gradient corresponds to the abso- spectrum after one of its most famous investiga- lute viscosity of the water, η. That is, tors (Kolmogorov, 1941), the impact of the lower η = τ / −1 end of the series on the behaviour of plankton (du dz) (2.1) had remained philosophically and mathemati- Adopting the appropriate SI units for force (N = cally obscure. My cumbersome attempts to over- newtons, being the product, mass × acceleration, come this deficiency in an earlier text (Reynolds, may be expressed as kg m s−2)per unit area (m2), 1984a)only emphasise this frustration. Looking for velocity (m s−1) and for vertical distance (m), back from the present standpoint, they serve theabsolute viscosity is solved in poises (P = as a point of reference for just how far the kg m−1 s−1). The values plotted in Fig. 2.1b approx- appreciation and quantification of turbulence, imate to 10−3 kg m−1 s−1.Caution over units is together with their impacts on particle entrain- urged because it is common in hydrodynamics ment, have moved on during the subsequent cou- to work with the kinematic viscosity of a fluid, ν, ple of decades. which is equivalent to the absolute viscosity with ‘Turbulence’ testifies to the failure of the the density (ρw)divided out: molecular structure of a fluid to accommodate −1 −1 2 −1 introduced mechanical energy. The mysteries ν = η (ρw) = τ(ρw du/dz) m s (2.2) TURBULENCE 45

Figure 2.5 The generation of turbulence by shear forces. In The transition between ordered and turbulent (a), the water beneath the horizontal surface is unstressed flow patterns has long been supposed to depend and at rest. In (b), a mild force, τ,isapplied which that drags upon the ratio between the driving and viscous water molecules at the surface in the direction of the force; forces; thisratioisexpressedby the dimension- (b) their movement serves to drag those immediately below, less Reynolds number, Re: and so on, giving rise to an ordered structure of laminar flow. In (c), the transmitted energy of the intensified force can no −1 −1 Re = (ρwula)η = ulaν (2.3) longer be dissipated through the velocity gradient which breaks down chaotically into turbulence. Redrawn, with where l is the length dimension available to permission, from Reynolds (1997a). a the dissipation of the energy, usually the depth of the flow. Turbulence will develop wherever there is a sufficient depth of flow with suffi- Given the density of water of ∼103 kg m−3 cient horizontal velocity. Solving Eq. (2.3)fora (Fig. 2.1a), its kinematic viscosity approximates notional small stream travelling at 0.1 m s−1 in a to 10−6 m2 s−1. channel 0.1 m deep, Re ≈ 104;fora10-mm layer If the applied force is now increased suffi- in a well-established thermocline in a small lake ciently, it begins to shear molecules from the subjected to a horizontal drift of 10 mm s−1, upper surface of the water column. Thus, the Re ≈ 102. The former is manifestly turbulent smooth, ordered velocity gradient fails to accom- but the latter maintains its laminations. There modate the applied energy; the structure breaks is no unique point at which turbulence develops up into a complex series of swirling, recoiling or subsides; rather there is a transitional range eddies (Fig. 2.5c). A new, turbulent motion is super- which, for water, is equivalent to Reynolds num- imposed upon the original direction of flow. bers between 500 and 2000. The depth–velocity The layer now assumes a net mean velocity in dependence of turbulence is sketched in the samedirection (¯u ms−1). Now, at any given Fig. 2.6. point within the turbulent flow, there would be The point in the spectrum where the eddies detected a series of velocity fluctuations, acceler- are overwhelmed by molecular forces and col- ating to (¯u + u)anddecelerating to (¯u − u) lapse into viscosity is more difficult to pre- ms−1.Simultaneously, the displacements in the dict without information on their velocities. vertical (z)direction introduce a velocity compo- As suggested above, it is now possible to mea- nent which fluctuates between (0 + w)and(0− sure the velocity fluctuations directly with the w)ms−1. This pattern is maintained for so long aid of sophisticated accoustic sensors but the as the appropriate level of forcing persists. The quantities still need to be interpreted within a driving energy is, as it were, extracted into the theoretical context. More significantly, the the- largest eddies, is progressively dissipated through oretical framework can be used estimate the smaller and smaller eddies of the Kolmogorov intensity of the turbulence from properties of spectrum and is finally discharged as heat, as the theflow which are measurable with relative smallest eddies are overwhelmed by viscosity. ease. 46 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

10 Figure 2.6 The onset of turbulence as a function of velocity and water depth. The boundary is 1 not precise, occurring at Reynolds numbers between Re = 500 and Re = 2000. Plot based on Reynolds Re = 2000 Turbulent 0.1 (1992b) and redrawn, with

Depth, H / m Transition Laminar permission, from Reynolds (1997a). Re 0.01 = 500

0.001 0.01 0.1 1 Velocity, u / m s−1

2.3.2 Quantifying turbulence coefficient of frictional drag on the surface (∼1.3 − The key empirical quantification of turbulence × 10 3). The equation is imprecise for a number is based upon the time-averaged velocity fluctu- of reasons, one being the interference in trans- ations in the horizontal and vertical directions fer caused by surface waves. Nevertheless, the ∗ (±u, ±w). Because the summation of positive implied linear relationship, (u ) ≈ U/800, is suffi- − and negative measurements must tend quickly ciently robust in the wind speed range 5–20 m s 1 ∗ − − − to zero, the positive roots of their squares, (u ∼6 × 10 3 to 2.5 × 10 2 ms 1)forit to stand [(±u)2]1/2,[(±w)2]1/2,arecumulated instead. The as a good rule-of-thumb quantity. turbulent intensity,(u∗)2, comes from the product Ageneral derivation for water flowing down a ∗ of their root mean squares: channel in response to gravity relates (u )to¯u,as ∗ / / − has been developed, inter alia,bySmith(1975): (u )2 = [(±u )2]1 2[(±w )2]1 2 m2 s 2 (2.4) ∗ −1 −1 (u ) = u¯[2.5ln(12H /rp)] ms (2.6) The square root (u∗) has the dimensions of velocity and is known variously as the turbulent velocity, where H is the depth of the flow and rp is the the friction velocity or the shear velocity.Innatural roughness of the bed, as defined by the heights of systems, both (u∗)and(u∗)2 are extremely vari- projections from the bottom. The ratio between ∗ able, in time and in space, depending upon the them is such that (u )isgenerally 1/30 to 1/10 ∗ energy of the mechanical forcing and the speed the value ofu ¯.Ageneral relationship relating (u ) at which it is dissipated through the eddy spec- to channel form is: trum. By considering the effects of forcing in con- ∗ / − (u ) · [g(A /p)s ]1 2 ms 1 (2.7) trasted situations, relevant ranges of values for x b ∗ −2 (u )maybenominated. where g is gravitational acceleration (in m s ), sb −1 Thus, the simplest model that may be pro- is the gradient of the bed (in m m ), Ax is the posed applies to a body of open water, of infi- cross-sectional area of the channel (in m2)andp nite depth and horizontal expanse and lacking is its wetted perimeter (in m). In wide channels any gradient in temperature. We subject it to a Ax/p approximates to the mean depth, H. Thus, (wind) stress of constant velocity and direction. ∗ / − (u ) · [gHs ]1 2 ms 1 (2.8) The momentum transferred across the surface b must balance the force applied. So we may pro- The turbulent velocity in a river 5 m deep and pose the following equalities: falling 0.2 m in every km, approximates to (u∗) = −2 −1 2 ∗ 2 −2 −2 10 ms .Turbulent intensity increases in rivers τ = ρacdU = ρw(u ) kg m s (2.5) with increasing relative roughness, with increas- −3 where ρa is the density of air (∼1.2 kg m ), U ing depth and increasing gradient. Theoretical is the wind velocity (properly, measured 10 m contours of (u∗)aremapped in Fig. 2.7 in terms above the water surface) and cd is a dimensionless of gradient and water depth and links them to TURBULENCE 47

Figure 2.7 Contour map of the approximate distribution of u∗ in aquatic environments (including rivers), in terms of water-column height, bed gradient and applied wind velocity. Original plot from Reynolds (1994b) and redrawn, with permission, from Reynolds (1997a).

those driven by surface wind stress: the dog-legs ished. For the wind-stirred boundary layer, with thus represent the ‘switch points’, where atmo- avertical velocity gradient, (du/dz), spheric forcing overtakes gravitational flow as the (u∗) ≈ l (du/dz)ms−1 (2.9) main source of turbulent energy in the water. e Major aquatic habitats are noted on the map. Even in the open ocean, the wind-mixed layer rarely extends more than 200–250 m from the surface (Nixon, 1988; Mann and Lazier, 1991). It is 2.3.3 Turbulent dissipation clear that so long as the inputs remain steady, the Before proceeding to the comparison of (u∗)with boundary-layer structure serves to dissipate the sinking velocities of plankters (us), it is helpful input of kinetic energy through the spectrum of to grasp how the turbulent energy runs down subsidiary eddies. The rate of energy dissipation, through the eddy spectrum and how this, in E,alsoturnsout to be an important quantity in turn, sets the environmental grain.Intrulyopen plankton ecology. Dimensionally, it is equivalent turbulence, the largest eddies generated should to theproduct of the turbulent intensity and the propagate smoothly into smaller ones, having velocity gradient. Thus, progressively lesser velocities as well as lesser ∗ − − − E = (u )2 (du/dz)m2 s 2 ms 1 m 1 (2.10) dimensions. Momentum is lost until the residual inertia is finally overcome once again by vis- By rearranging Eq. (2.9)for(du/dz) and substitut- cosity and order returns. In the absence of any ing for it in Eq. (2.10), it follows that: constraining solid surfaces (shores or bottom) or ∗ − − E ≈ (u )3l 1 m2 s 3 (2.11) density gradients, it is possible to envisage a e structure in which the largest eddies are adjacent Where the vertical dimension is constrained, to thesource of their mechanical forcing (such however, either because the basin is considerably as wind stress on the water surface) and a layer less deep than 250 m in depth or because den- of active, propagating turbulence (in this case, sity gradients resist the downward eddy prop- from the surface downwards), until the turbu- agation, the smaller surface mixed layer must lence is finally overwhelmed some distance away still dissipate the turbulent kinetic energy within (in this case, its lower base). The entire struc- the space available. Were this not so, the motion ture might then be regarded as a single bound- would have to spill out of the containing struc- ary layer, separating the energy source from the ture in, for instance, breaking waves or some non-energised water. The mechanical properties rapid erosion of the perimeter shoreline. What of the boundary layer then relate to the sizes of happens is that the residual energy reaches into the dimensions of the largest eddies (le)andthe smaller eddies before it is overcome by viscosity. gradient with which their velocities are dimin- Thus it is that the most relevant feature of the 48 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

∗ Ta b l e 2.2 Shear velocity of turbulence (u ), mixed-layer thickness (hm), dissipation rate (E) and smallest eddy size (lm)for various kinetic systems. Abstracted from the compilation of Reynolds (1994a).

∗ −1 2 −3 Site (u )(ms ) hm (m) E (m s ) lm (mm) Bodensee winter 6.2 × 10−3 to 44 to 177 1.4 × 10−8 to 2.9 to 1.5 winds, 5–20 m s−1 2.5 × 10−2 2.2 × 10−7 summer winds, ≤1 × 10−3 ≤20 ≤1.3 × 10−7 ≥1.7 <8ms−1 Lough Neagh winds, 1.3 × 10−2 to 8.9 5.4 × 10−7 to 1.2 to 0.7 10–20 m s−1 2.5 × 10−2 4.3 × 10−6 Ashes Hollow ≤3.1 × 10−1 0.05 ≤1.5 × 10−6 ∼0.9 (hill stream) River Thames ≤9.4 × 10−3 4.1 5.1 × 10−7 ∼1.2 (Reading) Open ocean ≤3.3 × 10−2 ≤233 ≤3.8 × 10−7 1.27 Shelf water (Irish Sea) ≤1.2 × 10−1 ≤100 ≤ 4 × 10−5 >0.4 Tidal estuary (Severn) spring ≤1.3 × 10−1 ≥10 ≤5.5 × 10−4 ≥0.20 neap ≥4.3 × 10−2 ≤40 ≥5.0 × 10−6 ≤0.67

physical environment of plankton is determined ratesofdissipation, and here the smallest eddies not by the intensity of mechanical energy intro- may be in the range 200–400 µm. duced but by the rate of its dissipation and the sizes of the smallest eddies that it can sustain. Simply, the greater is the rate of dissipation, the 2.3.4 Turbulent embedding of finer is the structural grain. phytoplankton In much the same way, we can deduce that These considerations are directly comparable the size ofthesmallest eddies (lm)inastructure with the dimensions of phytoplankton (Box 1.2, is independent of the forcing but depends only Tables 1.2, 1.7). Microplanktic algae are smaller, on the rate of energy dissipation (work) per unit by one or more orders of magnitude, than the mass (E,inJkg−1 s−1, which cancels to m2 s−3; smallest eddy sizes in what are arguably among see glossary of units, symbols and abbreviations) themost aggressively mixed, fastest dissipat- and the kinematic viscosity (ν,inm2 s−1): ing turbulence fields that they might inhabit. There are some observations and the evidence of 3 1/4 lm = (ν /E ) m (2.12) some experiments (Bykovskiy, 1978)that together suggest larger species of phytoplankton do not Solutions of Eq. (2.12)rangefrom the order of tolerate eddy diminution and intensified shear millimetres in mixed layers, extending to metres implicit in enhanced, fine-grained turbulence in stratified layers (Spigel and Imberger, 1987). fields but are, instead, readily fragmented. It is According to the data on well-mixed systems com- an unverified hypothesis to argue that phyto- piled by Reynolds (1994a), some of which are plankton have evolved along lines that exploited reproduced here as Table 2.2,the smallest eddy theviscous range of the aquatic eddy spectrum, sizes calculated to be experienced in oceans and rather than to have invested in the mechanical deeper lakes are hardly smaller than 1.3 mm. tissue necessary to resist the collapse and frag- In rivers and shallow lakes, the smallest eddies mentation of larger structures (Reynolds, 1997a). may be are only half as large for the same input If the dominant vegetation of pelagic environ- of kinetic energy. Tidal mixing of estuaries and ments is truly selected by its ability to escape the coastal embayments powers some of the fastest smallest scales of turbulence, then the corollary PHYTOPLANKTON SINKING AND FLOATING 49 is that the individual organisms are, in effect, to thepower generation of its saturated rate of embedded deep within the turbulence structures photosynthesis (∼1.4 kW kg−1). If it stops oper- to which the water has frequently to accom- ating its flagella, however, the alga comes to a modate. This is worth emphasising: planktic complete rest in ∼1 µs, having travelled no more algae live most of their lives in an immedi- than another 10 nm (10−8 m) in relation to the ate environment that is wholly viscous but, at adjacent medium (Purcell, 1977). aslightly larger scale, one that is simultane- Embedding is directly relevant to the issues of ously liable to be transported far and rapidly entrainment and distribution of phytoplankton, through the turbulence field, and with vary- insofar as the behaviour of the plankter relative ing intensity and frequency. The pelagic world toabody of water in motion is strongly influ- of phytoplankton might be analogised to one enced by the behaviour of the plankter within of little viscous packets being moved rapidly in its immediate viscous environment. To progress any of three dimensions. In reality, the pack- this exploration requires us to account for buoy- ets have no enduring integrity but it is the ancy and gravitation behaviour in relation to behaviour of phytoplankton relative to the imme- suspension. diate water and to the transport of the water within the mixed layer that determines the suspension and settling characteristics of the whole 2.4 Phytoplankton sinking and population. floating The consequences of living in a viscous medium have been graphically recounted in amuch-celebrated paper by Purcell (1977). For The buoyant properties of non-motile plankters, instance, it is not possible for a planktic alga having rigid walls but lacking flagella or cilia, or bacterium to ‘swim’ through the medium as moving through a column of water, in response = −2 does (say) a water beetle (3–20 mm), by means of to gravity (g 9.8081 m s ), are subject to the areciprocating, rowing movement of paddle-like same forces that govern the settlement of inert limbs, any more than can a man floundering in a particles in viscous fluids, which were quantified vat of treacle. The alternative options for forward over a century and a half ago (Stokes, 1851). As the progression that are exploited by microplank- body moves, it displaces some of the fluid. Pro- ters and smaller organisms include the serial vided the movement of the displaced fluid over deformation of the protoplast (amoeboid move- theparticle is laminar, thus causing no turbu- ment), the spiral rotation of the body (as do lent drag, then its velocity (ws)isrelated to its many ciliates and euglenoids) and the rotating size (diameter, d) and the difference between its ρ of a flagellum like a corkscrew (as in the bac- density from that of the water ( w). For a spheri- ρ terium Escherichia). The speed of self-propulsion cal particle of uniform density ( c), relative to the medium (us)of(say) a Chlamy- 2 −1 −1 ws = gd (ρc − ρw)(18 η) ms (2.14) domonas cell, 10 µmindiameter (d), is, at about 10 µms−1,trivial in absolute terms though nev- This is the well-known Stokes equation. Note ertheless impressive in body-lengths covered per that for a buoyant particle (ρc <ρw), Eq. 2.14 second. The Reynolds number of its motion per has a negative solution, representing a rate of second, solved by analogy to Eq. (2.3), confirms flotation upwards. An empirical verification by that the alga moves smoothly through the water, McNown and Malaika (1950), who measured the its motion creating no turbulence: sinking rates of machined metal shapes in viscous oils, is also frequently cited in the litera- = ρ η−1 Re ( wusd) ture on phytoplankton. The Stokes equation is ≈ 10−4 (2.13) implicitly taken as a valid base for predicting thesinking behaviour of phytoplankton but it is The power required to maintain this momentum, necessary also to test all its assumptions and com- ∼0.5 W kg−1,isalsoquitetrivial when compared ponents if we are to grasp the many mechanisms 50 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

that distort the relationship when applied to liv- otherwise known as form resistance. The effect ing organisms of other than spherical shapes. of departure from spherical form was clearly demonstrated by the experiments of McNown 2.4.1 Planktic movement and laminar flow and Malaika (1950). In most instances (the Let us take the condition of laminar flow. ‘teardrop’ shape being a notable exception), sub- McNown and Malaika (1950)showed good adher- spherical metal shapes sank through oil more ence to the Stokes formulation whilst Re < 0.1 slowly than the sphere of the same volume. It and that the error was <10% for Re < 0.5. For is difficult to account quantitatively for these comparison, Walsby and Reynolds (1980)applied results, as mathematical theory is not so well published data for phytoplankton to solve Eq. developed that the effects of distortion can (2.13)forvarious phytoplankton, approximating be readily calculated. However, McNown and 3 −3 −3 −1 −1 ρw as 10 kg m and η as 10 kg m s in each Malaika (1950) also published their findings on case. For the large marine centric diatom Coscin- thesinking of spheroids, both oblate (flattened odiscus wailseii (d ∼150 × 10−6 m), and substitut- in one axis, like a medicinal pill, or what British −3 −1 ing ws = 0.1 × 10 ms for us (from Smayda, readers will understand as ‘Smartie’-shaped) or 1970), Eq. (2.13)wasbalanced by Re = 0.015. prolate (shortened in two axes, towards the shape Similarly, using measurements from Reynolds of classic airships). These have provided plank- (1973a)forafreshwatercentric diatom, Stephan- tonscientists with an important foundation on −6 −6 odiscus rotula (d ∼50 × 10 m, ws = 25 × 10 theimpacts of form on algal sinking. Some inter- ms−1), Re = 0.00125. The deduction that esting theoretical or experimental investigations the movements of most phytoplankton comfort- have been pursued using cylinders (Hutchinson, ably conform to the laminar flow condition 1967;Komar, 1980), chains of spheres (Davey and is, however, challenged by very large plankters. Walsby, 1985) and, more recently, some inge- According to Smayda’s (1970)data,thesink- nious alga-like shapes fashioned in polyvinyl chlo- ing of the extraordinary Ethmodiscus rex,one ride (PVC) or malleable ‘Plasticine’ (Padisak´ et al., of the largest known diatoms (d ∼ 1mm, 2003a). These have helped to amplify an under- −3 −1 ws = 6 × 10 ms ), generates an Re ∼ 6. Work- standing of the importance of shape in the ing with a size range of colonies of the Cyanobac- behaviour of phytoplankton. terium Microcystis,Reynolds(1987a)showedthat In the case of spheroids, the reduction in sink- theStokesequation (2.14)predicted velocities ing is related to the ratio of the vertical axis = well in colonies of known densities up to (d ) (say, a)tothe√ square root of the product of the 200 × 10−6 mindiameter,butinlargercolonies other two ( bc). The fastest-sinking spheroid is (d up to 4 mm), velocities became significantly one in which a ≈ 2b and b = c:the horizon- overpredicted especially when Re > 1. tal cross-sectional area is smaller than that of the sphere ofthesamevolume but with most 2.4.2 Departure from spherical shape: of the volume in the vertical where it offers form resistance less drag, the spheroid actually sinks faster√ than If the laminar-flow condition may thus be the sphere. As the ratio is increased [a/( bc)to assumed to apply to the movements of micro- >3], drag increases and velocity falls below that phytoplankton, probably at all times, it is not of the equivalent√ sphere. Analogously, making at all clear that the Stokes equation can apply a < b and a/( bc) < 1, drag increases more other than to spherical organisms, coenobia or than the horizontal cross-sectional area and to colonies, less than 200 µmindiameter. In fact, >3. Spheroids with the most disparate diameters, forthe majority of phytoplankters that are not that is, the narrower or the flatter they are with spherical, the shape distortion has a significant respect to the sphere of identical volume and impact on the rate of settling. Distortion from the density, offer increased form resistance and up sphere inevitably results in a greater surface area toatwofold reduction in sinking rate. to an unchanged volume and density and, hence, In the case of cylinders, increasing the agreater volume-specific frictional surface, length but keeping the cross-sectional diameter PHYTOPLANKTON SINKING AND FLOATING 51

constant increases sinking velocity, although this the calculated rate of sinking (ws calc) with the approaches a maximum when length exceeds observed rate of sinking by direct measurement, diameter about five times. Cylinders at this criti- ws. Thus, cal length have about the same sinking speed as ϕ = / spheres of diameter 3.5 times the cylinder sec- r ws calc ws (2.15) tion (d ). As a cylinder having a length of 7(d ) c c The Stokes equation should also be modified in has the same volume as such a sphere, we may respect of phytoplankton (Eq. 2.16)byincluding a deduce that cylinders relatively longer than this term forform resistance, accepting that the value will sink more slowly than the equivalent sphere, of ϕ may be so close to 1 that the estimate pro- so long as all other Stokesian conditions are ful- r vided by Eq. (2.14)would have been acceptable. filled. It has been suggested in several earlier stud- 2 −1 −1 ws = g(ds ) (ρc − ρw)(18 ηϕr) ms (2.16) ies that distortions in shape have another role in orienting the cell, that (for instance) the cylin- This approach allows systematic variability in the drical form makes it turn normal to the direc- coefficient to be investigated as a feature of phy- tion of sinking and that this may be advan- toplankton morphology. Some of the interesting tageous in presenting the maximum photosyn- findings that impinge on the evolutionary ecol- thetic area to the penetrating light. Walsby and ogy of phytoplankton are considered in the next Reynolds (1980)argued strongly for the counter- section but it is important first to mention the view. In a truly turbulence-free viscous medium, practical difficulties that have been encountered ashape should proceed to sink at any angle at in estimating form resistance in live phytoplank- which it is set. There is an exception to this, ton and the ways in which they have been solved. of course, which will apply if the mass distribu- As observed elsewhere (Chapter 1)preciseesti- tion is significantly non-uniform: the ‘teardrop’ mates of the volume of a plankter (whence ds reorientates so that it sinks ‘heavy’ end first. In is calculable) are difficult to determine if the the experiments of Padisak´ et al.(2003a), some of shape is less than geometrically regular. Making the models of Tetrastrum were made deliberately a concentrated suspension and determining the unstable by providing spines on one side only: volume of liquid it displaces offers an alterna- these, too, reoriented themselves on release but tive to careful serial measurements of individu- then remained in the new position throughout als. Walsby and Xypolyta (1977)gavedetails of a the subsequent descent. Their observations on procedure using 14 C-labelled dextran to estimate Staurastrum models that go on reorienting recalls theunoccupied space in a concentrated suspen- the observations of Duthie (1965)onrealalgae of sion. The usefulness of the approach neverthe- this genus, which reorientated persistently dur- less depends upon a high uniformity among the ing descent to the extent that they rotated and organisms under consideration – cultured clones veered away from a vertical path. At the time, the are more promising than wild material in this influence of convection on the sinking behaviour respect. of Staurastrum could not be certainly excluded. The densities of phytoplankton used to be dif- The results of Padisak´ et al.(2003a)suggest that ficult to determine precisely, having to rely on the form ofthecells engenders the behaviour as good measurements of mass as well as of vol- it reproduced in a viscous medium. ume. Now, it has become relatively easy to set up For the present, the impact on sinking of dissolution gradients of high-density solutes, intro- tortions as complex as those of Fragilaria or Pedi- duce the test organisms then centrifuge them astrum coenobia requires more prosaic methods until they come to rest at the point of isopycny of assessment. The most widely followed of these between the organism and solute (Walsby and is to calculate a coefficient of form resistance (ϕr) Reynolds, 1980). Following Conway and Trainor by determining all the variables in the Stokes (1972), Ficoll is frequently selected asanappropri- equation (2.14)forasphereofequivalentvol- ate solute. Being physiologically inert and osmot- ume (having the diameter, ds)andcomparing ically inactive improves its utility. 52 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Even to get accurate measurements of sinking rate (ws)isproblematic. Here, the main issue is to be able to keep the water static, when almost any conventional observation system involving uninsulated light sources is beset by generated convection. Techniques have been developed or applied, using some combination of strict ther- mostatic control, thin observation cells (Wise- man and Reynolds, 1981)ornon-heat-generating measuring systems based on fluorometry (see, for instance, Eppley et al., 1967;Tilman and Kilham, 1976;Jaworski et al., 1981). Another approach has been to make measurements in solutions of high viscosity: Davey and Walsby (1985)usedglycerol. Alternatively, to measure the rate of loss across aboundary layer from an initially mixed suspension works with convection and yields acceptable results on field-collected material when sophisticated techniques may not be readily available (Reynolds et al., 1986). This actually imitates, in part, the way that plankton settles from natural water columns (see Section 2.6). Once confidence was gained in the measure- Figure 2.8 Log/log plot of the instantaneous intrinsic ment of sinking rates, another, more tantalising settling rates (ws)ofStephanodiscus rotula cells, collected from ◦ source of variability was detected. Several, quite the field and plotted against mean cell diameter, ds ( ). There is apparently no correlation. However, when corresponding independent investigations of the species-specific samples are killed by heat prior to determination ( t), a strong sinking rates of diatoms each yielded order-of- positive correlation is found. Redrawn from Reynolds (1984a). magnitude variability. For any given species, the sinking rates seemed least when the cells were healthy and physiologiclly active but were as phytoplankton was to first kill the diatoms under much as three to seven times faster in similar test.Acase in point is shown in Fig. 2.8, where cells that were naturally moribund (Eppley et al., the meansinking rates of Stephanodiscus rotula 1967;Smayda, 1970;Reynolds, 1973a), or whose cells sampled during the increase and decrease photosynthesis was experimentally inhibited or phases of a natural lake population seem to vary carbon-limited (Jaworski et al., 1981), or which randomly. However, the corresponding rates of had been exposed to sublethal doses of algi- cells killed by dipping in boiling water just before cide (Margalef, 1957;Smayda, 1974), or had been measurement were demonstrably correlated to otherwise freshly killed (Wiseman and Reynolds, size. It is now quite generally accepted that live, 1981). However, comparing the fastest rates from healthy diatoms have the capacity to lower their each of the studies that had made measure- sinking rates below that of dead or moribund ments on comparable material (eight-celled stel- ones. The mechanism of change is not obviously late coenobia of the freshwater diatom Asteri- contributed by variability in size or shape or even onella formosa), some conformity among the var- density. Sinking of live diatoms and, possibly, ious results became apparent (Jaworski et al., other algae is plainly influenced by the interven- 1988). tion of further, vital components that must be Wiseman et al.(1983) had previously estab- taken into account in any judgement on how phy- lished that the one sure way to get the consistent, toplankton regulate their sinking rates. inter-experimental results necessary to be able to To go on now to review some of the ana- investigate the morphological form resistance of lytical investigations into the sinking rates of ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 53 phytoplankton and the role of form resis- by a relatively greater silicon content. However, tance provides the simultaneous opportunity it is probable that the effect is enhanced by the to observe the cumulative influences of the fact that a relatively greater part of the inter- biotic components of the modified Stokes equa- nal space of larger diatoms is occupied by cell tion (2.16). sap rather than cytoplasm (Walsby and Reynolds, 1980)and that many marine diatoms, at least, are known to be able to vary the sap density rela- 2.5 Adaptive and evolutionary tive to that of sea water (Gross and Zeuthen, 1948; Anderson and Sweeney, 1978). This mechanism of mechanisms for regulating ws density regulation is not available to freshwater algae (see Section 2.5.2) but, either way, density Of the six variables in the modified Stokes equa- effects may be vital to the suspension of larger ρ η tion, three (g, w and )areeitherconstants diatoms in the sea, if the reduction of sinking or are independent variables. The other three ratesisthe ultimate adaptive aim. According to (size, density and form resistance) are organismic Smayda’s (1970) data, cells of Coscinodiscus wailesii properties and, as such, are open to adaptation should settle at a rate of 40 m d−1, had they the and evolutionary modification through natural same net density as the much smaller Cyclotella selection. It is possible that certain metabo- nana,rather than the observed 8–9 m d−1. lites released into the water by organisms also affect the viscosity of the adjacent medium. The 2.5.2 Density present section looks briefly at the influences The cytoplasm of living cells comprises compo- of each on sinking behaviour and the extent to nents that are considerably more dense than which a planktic existence selects for particular water (proteins, ∼1300; carbohydrates, ∼1500; adaptive trends. nucleic acids ∼1700 kg m−3), so that the average density of live cells is rarely less than ∼1050 2.5.1 Size kg m−3. Inclusions such as polyphosphate bodies The relatively small size of planktic algae has (∼2500 kg m−3) and exoskeletal structures of cal- been alludedtoinChapter1.Forinstance, the cite and, especially, the opaline silica of diatom diameters of the spheres of equivalent volumes to frustules (∼2600 kg m−3)increase the average species named in Table 1.2 cover a range from 1 density still further. Some of the excess density to 450 µm. It has been suggested that this is itself can be offset by the presence of oils and lipids an adaptive feature for living in fine-grained tur- that are lighter than water, the lightest having a bulence. Many species may present rather greater density in the order of 860 kg m−3 (Sargent, 1976). maximal dimensions if (presumably) the rate of However, these oils rarely account for more than turbulent energy dissipation allows. The effect of 20% of the cell dry mass. Without adaptation, size on the settling velocities of centric diatoms most freshwater phytoplankters are bound to be was demonstrated empirically by Smayda (1970). heavier than the medium and naturally sink! The Astriking feature of his regression of the loga- corresponding deduction in respect of marine rithm of velocity ws on the average cell diameter phytoplankton suspended in sea water (ρw gener- (d)isthatitsslopelies closer to 1 than 2, as would ally ∼1030 kg m−3)ismadewith rather less con- have been expected from the Stokes equation fidence, where the scope for regulation of ρc can (2.14). The regression fitted to the plot of sink- be more purposeful. ing rates ofkilled Stephanodiscus cells against the The list in Table 2.3 is an abbreviated version diameter (in Fig. 2.8)alsohasaslopeof∼1.1. The of one that was included in Reynolds (1984a). It observations suggest that the larger size (and, is intended to illustrate the range of densities hence, the larger internal space) is compensated rather than the comprehensiveness of the data. by alower overall unit density (cf. Section 1.5.2 In particular, it is easy to distinguish the gas- and Fig. 1.9). The implication is that more of the vacuolate Cyanobacteria which, in life, have den- overall density of the small diatom is explained sities of ≤1000 kg m−3 that enable them to float, 54 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Ta b l e 2.3 Some representative determinations of phytoplankton densities

a Species ρc (range, in Method References kg m−3) Cyanobacteria Anabaena flos-aquae 920–1030b 1 Reynolds (1987a) Microcystis aeruginosa 985–1005b 1 Reynolds (1987a) (colonies) Planktothrix agardhii 985–1085b 1 Reynolds (1987a) Chlorophyta Chlorococcum sp. 1020–1140 2 Oliver et al.(1981) Chlorella vulgaris 1088–1102 2 Oliver et al.(1981) Bacillariophyta Stephanodiscus rotula 1078–1104 3 Reynolds (1984a) Synedra acus (culture) 1092–1138 2 Reynolds (1984a) Thalassiosira weissflogii 1121 3 Walsby and Xypolyta (1977) Tabellaria flocculosa 1128–1156 2 Reynolds (1984a) Asterionella formosa 1151–1215 2 Wiseman et al.(1983) Fragilaria crotonensis 1183–1209 2 Reynolds (1984a) Aulacoseira subarcticac 1155–1183 2 Reynolds (1984a) Aulacoseira subarcticad 1237–1263 2 Reynolds (1984a)

a Methods: (1) calculations based on experimental changes in velocity and gas-vesicle content (see text); (2) deteminations by centrifugation through artificial density gradient to isopycny; (3) gravimetric determinations of mass and volume. b Range covers colonies or filaments with maximum known gas vacuolation to colonies or filaments after subjection to pressure collapse (see text). c Post-auxosporal (wide filaments). d Pre-auxosporal (narrow filaments). All measurements on wild material, unless otherwise stated.

but which are heavier than fresh water if the Lipid accumulation vesicles are collapsed by pressure treatment (see Fats and oils normally account for some 2–20% of below). Two, small unarmoured chlorophytes are the ash-freedrymassof phytoplankton cells, per- included (data of Oliver et al., 1981); how typical haps increasing to 40% in some instances of cel- they are of non-siliceous algae is not known. The lular senescence (Smayda, 1970;Fogg and Thake, silica-clad diatoms have densities generally ≥1100 1987). Most lipids are lighter than water and, kg m−3,although there is a good deal of vari- inevitably, their presence counters the normal ability. Interestingly, it seems likely that density excess density to some limited extent. Oil accu- varies inversely to internal volume (Asterionella vs. mulation is responsible for the ability of colonies Stephanodiscus,slender pre-auxosporal Aulacoseira of the green alga Botryococcus to float to the vs wide post-auxosporal cells). surface in small lakes and at certain times of Apart from these generalisations, average den- population senescence (Belcher, 1968). However, sities of many planktic algae are plainly influ- it is improbable that oil or lipid storage could enced by a number of discrete mechanisms. reverse the tendency of diatoms to sink. Reynolds These include lipid accumulation, ionic regula- (1984a) calculated that were the entire internal tion, mucilage production and, in Cyanobacteria, volume of an Asterionella cell to be completely the regulation of gas-filled space. filled with the lightest known oil, its overall ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 55 density (∼1005 kg m−3)would still not be enough scope for ionic regulation in phytoplankton of −3 to make it float. Walsby and Reynolds (1980) con- freshwater (ρw < 1002 kg m )istoonarrowto cluded that the reduction in density consequen- be advantageously exploited. tial upon intracellular lipid accumulation would, unquestionably, contribute to a reduced rate of Mucilage sinking but they doubted any primary adaptive The mucilaginous investment that is such a com- significance, neither was there evidence of its use mon feature of phytoplankton, especially of fresh- as a buoyancy-regulating mechanism. water Cyanobacteria, chlorophytes and chrysophytes, has long been supposed to function as a buoyancy aid. Again, that mucilage does Ionic regulation reduce overall density is, generally, indisputable. Inherent differences in the densities of equimo- Whether this is a primary function is less cer- lar solutions of organic ions raise the possibil- tain (see Box 6.1, p. 271)anditis mathematically ity that selective retention of ‘light’ ions at the demonstrable that the presence of a mucilagi- expense of heavier ones could enable organisms nous sheath does not always reduce sinking rate; to lower their overall densities. In a classical in fact it may positively enhance it. paper, Gross and Zeuthen (1948) calculated the The presence, relative abundance and consis- density of the cell sap of the marine diatom Dity- tency of mucilage is highly variable among phylum brightwellii to be ∼1020 kg m−3,thatis,signif- toplankton. Mucilages are gels formed of loose icantly lower than the density of the suspending networks of hydrophilic polysaccharides which, sea water and actually sufficient to bring overall though of high density (∼1500 kg m−3)them- density of the live diatom close to neutral buoy- selves, are able to hold such large volumes of ancy. The density difference between sap and sea waterthat their average density (ρm)approaches water was explicable on the basis of a substantial isopycny. Reynolds et al.(1981)estimated the den- replacement of the divalent ions (Ca2+,Mg2+)by sity of the mucilage of Microcystis to average + + −3 monovalent ones (Na ,K )withrespect to their ρw + 0.7 kg m . The presence of mucilage can- concentrations in sea water. Some years later, not make the organism less dense than the sus- Anderson and Sweeney (1978)wereabletofollow pending water but it can bring the the aver- changes in the ionic composition of cell sap of age density of the cell or colony maintaining it Ditylum cells grown under alternating light–dark much closer to that of the medium (ρc). How- periods. They were able to show that density ever, the clear advantage that this might bring −3 may, indeed, be varied by up to ±15 kg m , to reducing ws in, for instance, Eq. (2.16)must through the selective accumulation of sodium or be set against a compensatory increase in over- potassium ions, though interestingly, not suffi- all size (ds is increased). Thus, for mucilage to ciently to overcome the net negative buoyancy be effective in depressing sinking rate, the den- of the cells. Elsewhere, Kahn and Swift (1978) sity advantage must outweigh the disadvantage were investigating the relevance of ionic regula- of increased size. tion to the buoyancy of the dinoflagellate Pyrocys- This relationship was investigated in detail by tis noctiluca;theyshowedthat by selective adjust- Hutchinson (1967). If a spherical cell of density, 2+ 2+ 2− ment of the content of Ca ,Mg and (SO4) , ρc,isenclosed in mucilage of density, ρm,such thealga could become positively buoyant. that its overall diameter is increased by a factor The effectiveness of this mechanism is not to a,thenitssinking rate will be less than that of be doubted but its generality must be regarded the uninvested cell, provided: with caution. For it to be effective does depend (ρ − ρ )/(ρ − ρ ) > a (a + 1) (2.17) upon maintaining a relatively large sap volume. c m m w The scope of density reduction is limited, in so Because a is always >1, the density difference farasthe dominant cations in sea water are the between cell and mucilage must be at least that lighter ones and the lowest sap density is the iso- between mucilage and water. Supposing ρc to be −3 tonic solution of the lightest ions available. The ∼1016 kg m , ρw to be 999 and ρm to be 999.7, 56 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

diameter of the sphere equivalent to the total volume of cells enclosed. The data presented appear to fall within the range of beneﬁt (in terms of sinking rate), although in the case of Pseudosphae- rocystis and some Coenochloris colonies, the ratios appear to unfavourable, at least if the assumptions about the component densities apply in all these cases.

Gas vacuoles The surest way of lowering average density is to maintain gas-filled space within the protoplast. This is precisely what some of the planktic Cyanobacteria do and, as is well known, the organisms become buoyant at times, accumulatu- ing at the surface as a scum, constituting what was originally called a ‘water bloom’. The term ‘bloom’ has since been applied to almost any planktic population (not even necessarily algal) significantly above the norm: it is another of Figure 2.9 The effect of mucilage thickness (a,asamultiple those words that has been misused to the point of ρ = ρ + ρ of diameter, ds)onthe average density ( c m)ofa being rendered unhelpful. However, the biology ρ = spherical alga of constant diameter and density ( c of scum-forming Cyanobacteria is a fascinating 1016 kg m−3). The arrow on the relative velocity plot topic, and not only because of the almost univer- indicates the point of maximum advantage of mucilage investment in the context of sinking-velocity reduction. sal contempt in which most environmental and Redrawn from Reynolds (1984a). water-supply managers hold their unsightliness and potential toxicity (Bartram and Chorus, 1999; see also Section 8.3.2). Part of the remarkable Eq. (2.17) can be solved as 23.3 > a (a + 1), or that account of the functional morphology and pop- a must be <4.3, if the presence of mucilage is ulation dynamics concerns the ability of these to reduce the sinking rate. The maximum advan- Cyanobacteria to regulate the buoyancy provided tage can be solved graphically (see Fig. 2.9); with by their gas vacuoles (Reynolds et al. 1987). Nested the nominated values, the greatest advantage within this is the unfolding appreciation of the occurs when a ∼ 2.3. Of course, the precise opti- structure and function of the buoyancy provision mal value of a varies from alga to alga, depend- itself. Much of the progress over the last 30 years ing partly upon the nature of the mucilage but has been spearheaded by A. E. Walsby and his co- mainly upon the cell density. For a diatom with workers. Walsby’s (1994)reviewisone of the most acelldensity of 1200 kg m−3,thegreatest value comprehensive, and it is this to which the reader of a that would bring a net reduction in its sink- is referred for all details. ing rate could be as high as 16.4, with maximum Here, it is sufficient to emphasise that, from advantage at a ∼ 8.7. thetime their existence was first established In order to compare the mucilage provision (Klebahn, 1895), gas vacuoles have been assumed among planktic algae, which are not all spheri- to have the function of providing buoyancy. cal, it is useful first to express cell volume as a Although this may have been neither their origi- proportion of the total unit volume (vc/vc+m,as nal nor their only function (Porter and Jost, 1973, included in Fig. 2.9). Some examples are given in 1976), these uniquely prokaryotic organelles cer- Table 2.4. In each instance, the range of values of tainly do reduce the average density of the cell a is calculated as the ratio of the diameter of the in which they occur. They are not bubbles – sphere equivalent to the full unit volume and the surface tension is much too powerful to permit ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 57

Ta b l e 2.4 Relative volumes of cell material (vc)asaproportion of the full unit volume (vc+m)ofnamed mucilage-producing phytoplankters, expressed in terms of Hutchinson’s (1967)factor a (see text)

Plankter vc/vc+m a References Microcystis aeruginosa 0.03–0.05 1.59–3.22 Reynolds et al.(1981) Anabaena circinalis 0.045–0.124 2.00–2.81 Previously unpublished measurements reported in Reynolds (1984a) Chlamydocapsa planctonica 0.126 1.99 Previously unpublished measurements reported in Reynolds (1984a) Coenochloris fottii 0.005–0.532 1.24–9.52 Previously unpublished measurements reported in Reynolds (1984a) Eudorina unicocca 0.055–0.262 1.64–2.63 Previously unpublished measurements reported in Reynolds (1984a) Pseudosphaerocystis lacustris 0.008–0.013 4.30–4.92 Previously unpublished measurements reported in Reynolds (1984a) Staurastrum brevispinum – 2.2–2.3 From direct measurements taken from Fig. 27 of Ruttner (1953) Fragilaria crotonensis 0.032–0.047 2.78–3.14 From direct measurements of linear dimensions taken from Plates 1c and 1d of Canter and Jaworski (1978), with calculation of a their existence at the scale of micrometres – but assembles. The structures are vulnerable to exter- rigid stacks of proteinaceous cylindrical or pris- nal pressure, including the internal turgor pres- matic envelopes called gas vesicles (Bowen and sure of the cell. They have a certain strength but, Jensen, 1965). In the Cyanobacteria, they gener- once a critical pressure has been exceeded, they ally measure between 200 and 800 nm in length. collapse by implosion. They cannot be reinflated; The diameters of isolated gas vesicles vary inter- they can only be built de novo,although the gas- specifically between 50 and 120 nm, but are rea- vacuole protein is believed to be recyclable. sonably constant within any given species. Each The critical pressures of isolated gas ves- molecule of the specialised gas-vesicle protein has icles are inversely correlated to their diameters ahydrophobic end and they are aligned in ribs in (Hayes and Walsby, 1986). The higher is the crit- the vesicle wall so that the entry of liquid water ical pressure of the vesicles, the greater the into the internal space is prevented. However, the hydrostatic pressure and, thus, the greater water vesicle wall is fully permeable to gases and in depth they can withstand. Intriguingly, vesicle no sense do the vesicles hold gas under anything size, like organism size and shape, co-varies with but ambient pressure. The gas inside the vesicles theprincipal ecological ranges in which individ- is usually dominated by nitrogen with certain ual species occur and, arguably, the habitats to metabolic by-products but it is clear that the gas which they are best adapted. In Anabaena flos- composition is of much less significance than is aquae,acommon scum-forming species in small the gas-filled space, which is created as the vesicle eutrophic lakes, vesicles measuring about 85 nm 58 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

in diameter have a critical pressure of 0.3 to 0.7 MPa (Dinsdale and Walsby, 1972). In Microcystis aeruginosa,aspeciessometimes found in larger and more physically variable lakes, vesicles averaging 70 nm in diameter have critical pressures in the order of 0.6–1.1 MPa (Reynolds, 1973b; Thomas and Walsby, 1985). The species of Plank- tothrix (formerly Oscillatoria)ofdeep, glaciated lakes in mountainous regions have vesicles measuring 60–65 nm that withstand pressures of between 0.7 and 1.2 MPa (Walsby and Klemer, 1974;Walsby et al., 1983;Utkilen et al., 1985a). Anabaena lemmermanni,aspecies more usually found distributed in the deep mixed layers of larger temperate lakes, also has much stronger vesicles than most other Anabaena species (0.93 MPa: Walsby et al., 1991). Vesicles from the oceanic Trichodesmium thiebautii were found to tolerate up to 3.7 MPa (Walsby, 1978). It is now recognised that gas-vesicle size is Figure 2.10 The relationship between sinking velocity (ws) − subject to very strong selective pressure. Narrow or floating velocity ( ws)ofcells of Anabaena circinalis and gas vesicles are less efficient at providing buoy- their gas-vacuole content as a proportion of cell volume. ancy and, for a given yield of gas-filled space, After Reynolds (1972) and redrawn from Reynolds (1984a). they are assembled at greater energetic cost. Nar- rower ones should only be selected if the extra tially linear relationship between density (and strength is required (Walsby and Bleything, 1988). buoyant velocity) and the gas-vacuole content. It Now that the genes controlling gas-vesicle assem- is ‘potential’ in so far as other items in the com- bly can be identified relatively easily (Beard et al., plement of cell materials affect the density, and 1999, 2000), the selection by hydrographic events the velocity is sensitive to size and form resis- (for instance, incidences of deep mixing of Plank- tance. Measurements of the gas-vesicle content tothrix populations) for the survival of relatively required to gain neutral buoyancy vary between more of the stronger or relatively more of the 0.7% and 2.3% of the cell volume (Reynolds and weaker kind is one of the most elegant demon- Walsby, 1975). strations of gene-based natural selection to have To conclude this very brief overview of the been contrived (Bright and Walsby, 1999;Davis buoyancy provision that gas vacuoles impart, it et al., 2003). is relevant to the ecology of these organisms to The buoyancy-providing role of the gas vesi- refer to the mechanisms of buoyancy regulation. cles has been studied for over 30 years. By prepar- To be continuously buoyant is arguably advan- ing very thick suspensions of Cyanobacteria, plac- tageous in deep, continuously mixed water lay- ing them in specific-gravity bottles and then ers. In small, possibly sheltered lake basins and subjecting them to pressures sufficient to colin larger ones at low latitudes, where the vari- lapse the vesicles, the volume of gas displaced ability in convective mixing is highly responsive can be measured very accurately. Expressed rel- to diurnal heat income and net nocturnal heat ative to the cell volume, the percentage of gas- loss, it is biologically useful to be able to alter or filled space is readily calculated (Walsby, 1971). even reverse buoyancy. There are at least three Reynolds (1972)usedthismethodtocollect the ways in which the planktic Cyanobacteria do data used to construct Fig. 2.10, which is included this. The relative content of gas vesicles is, in to show that there is, for any given alga, a poten- thefirst instance, the outcome of the balance ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 59 between their assembly and their collapse. As small differences in density (as predicted in the cells simultaneously grow and divide, gas vesicles modified Stokes equation, 2.16), allowing Micro- will be ‘diluted out by growth’ unless the cellular cystis colonies to migrate on a diel basis in stable resource allocation to their assembly keeps pace. water columns and to recover vertical position There is plenty of evidence (reviewed in Reynolds, very rapidly after disruptive storms. Apart from 1987a)that the processes are not closely coupled thefirst detailed descriptions of this behaviour in and that the relative content of vesicles increases shallow, tropical Lake George (Ganf, 1974a), simi- during slow (especially light-limited) growth and lar adjustments, the ability of Microcystis to attain decreases during rapid growth. It is also appar- this control on its buoyancy, is apparent from ent that for the species with the strongest vesi- thestudies of Okino (1973), Reynolds (1973b, cles, this is the main mechanism of control and, 1989a), Reynolds et al.(1981) and Okada and Aiba of course, it operates at the scale of genera- (1983). tion times. For the species with weaker vesicles No less striking is the formation of persistent that are vulnerable to collapse in the face of plate-like layers in the stable metalimnia of cer- rising turgor generated by low-molecular-weight tain relatively deep lakes: the plankters may be carbohydrates, there is a rather more respon- almost lacking from the water column but for sive mechanism of reversing buoyancy. Cells float- aband of 1 m or rather less, where they remain ing into higher light intensities photosynthesise poised, often at quite low light intensities. The more rapidly, raise cell turgor, collapse vesicles, behaviour has been known for many years from lose buoyancy, sink back where the cycle can alpine lakes in central Europe (Findenegg, 1947; start again. The cycle of buoyant adjustments can Thomas, 1949, 1950;Ravera and Vollenweider, operate on a diel basis and bring about daily 1968;Zimmermann, 1969;Utkilen et al., 1985a) migratory cycles over depth ranges of 2–4 m, and generally involves the solitary filaments cells accumulating near the surface by night and of Planktothrix of the rubescens–prolifica–mougeotii at greater depths by the end of the daylight group but it is also known from small, stratifying period (Reynolds, 1975;Konopka et al., 1978). Such continental lakes elsewhere (Juday, 1934;Atkin, behaviour may be invoked to explain the diel 1949;Eberley, 1959, 1964,Lund, 1959;Brook et migratory cycles of Anabaena spp. (reported by al., 1971,Gorlenko and Kuznetsov, 1972;Walsby Talling, 1957a;Pushkar’, 1975;Ganfand Oliver, and Klemer, 1974) and to involve other genera 1982)andAphanizomenon (Sirenko et al., 1968; (Lyngbya,orPlanktolyngbya, Spirulina:Reynoldset Horne, 1979), or imitated in laboratory mesocosm al., 1983a;Hinoet al., 1986). The ability to main- (Booker et al., 1976;Booker and Walsby, 1981). tain station is attributable to close regulation of The third mechanism can also result in fairly gas-vesicle content but the very low light inten- fine control of buoyancy trimming in Cyanobac- sities suggest that this is regulated by alloca- teria with gas vesicles of intermediate strength, tion. Zimmermann’s (1969)study showed that, such as those of Microcystis,beyond the scope of through the season, P. rubescens moves up and the turgor-collapse mechanism. Here, the buoy- down in the water column of Vierwaldstattersee,¨ ancy provided by a coarsely variable complement mainly in response to changes in the down- of robust gas vesicles is countered by a finely welling irradiance. The cells are able to main- variable accumulation of photosynthetic poly- tain biomass or even to grow slowly in situ and mers (chiefly glycogen) of high molecular weight thebehaviour has been interpreted as a sort of (Kromkamp and Mur, 1984; Thomas and Walsby, ‘aestivation’, to escape the period of minimal 1985). So long as approximate neutral buoyancy resource supply. However, the recent season-long is maintained, relatively small differences in the investigation by Bright and Walsby (2000)ofthe glycogen content take the average density of P. rubescens stratified in the Zurichsee,¨ points to a the colonies either side of neutral buoyancy, in sophisticated set of adaptations to gain positive response to insolation and photosyntetic rate. growth in the only region of the lake where a The large size attained by colonies magnifies the small nutrient base and a low light income are 60 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

simultaneously available. The ability to control strain, although there is a possibility that there organismic density is crucial to the exploitation wasadensitydifferencebetweenthetwoforms of the opportunity. (Conway and Trainor, 1972). However, the investigations of the role of the 70-nm chitin fibres that 2.5.3 Form resistance adorn the frustules of Thalassiosira weissflogii (for- Many plankters are markedly subspherical in merly T. f luviatilis)inslowingthesinking speed shape and theory suggests that, in a majority of cells have been carefully evaluated by Walsby of instances, the departure results in the organ- and Xypolyta (1977). Cells from which the fibres ism having a slower passive rate of sinking (or had been removed with a fungal chitinase sank floating) than the sphere of equivalent volume almost twice as fast as those not so treated, even and overall density. As has been suggested ear- though the density of the fibres (1495 kg m−3)was lier, there have really been few attempts to verify rather greater than that of the fibreless cells. The that this is true for a majority of species, and overall volume of the untreated cells was also then mainly through resort to empirical evalu- larger (1.9-fold) than that of the fibreless cells ation of the coefficient of form resistance, ϕr. but the surface area was 2.8 times greater. Only Even where significant form resistance is estab- theincreased form resistance could have been lished experimentally (see entries in Table 2.5), it responsible for the reduced sinking rate. does not prove distortion to be necessarily adaptive in the context of floating and sinking. Never- Chain formation theless, the experimental demonstrations of the Joining two or more cells together obviously impact on sinking rate made by the presence of increases the volume of the settling particle in horns or spines, cell elongation in one (or pos- the same ratio. It also increases the surface area, sibly two) axes and the creation of secondary but for the area of mutual contact between indi- shapes by coenobial formations of chains, fila- vidual cells in the chain. Theory dictates that ments and spirals make a fascinating study. In thechain must sink faster than the individual the end, theymayprovide the key to how larger component cells – were sinking rate the only plankters actually do maximise their suspension criterion, joining cells together could not be opportunities. claimed to be an adaptation to suspension. On theother hand, as pointed out by Walsby and Protuberances and spines Reynolds (1980), if there is another constraint The value of distortions to staying in suspen- favouring larger size (say, resistance to grazing), sion goes back a long way in planktology, cer- it is equally clear that the linear arrangement tainly to Gran’s (1912)interpretation, quoted by preserves much more surface drag than a sphere Hardy (1964), of a verifiable tendency for Ceratium of the same volume of the aggregate of cells. species of less viscous tropical seas to have longer Hutchinson (1967) invoked the results of some and, often, more branched horns than the species experiments by Kunkel (1948), who had mea- typical of colder, high-latitude seas. Yet it is only sured sinking rates of identical glass beads, either relatively recently that effects were quantitatively singly or cemented together in linear chains of demonstrated. Smayda and Boleyn (1966a)inves- one, two, three, four or eight. Hutchinson (1967) tigated several aspects of the variability in sink- calculated the relative form resistance and fit- ing rateinthemarinediatomRhizosolenia setigera, tedalinear plot against chain length with the including the fact that spineless pre-auxospore equation: cells settle significantly faster than the spined ϕ = 0.837 + 0.163b (2.18) vegetative cellsthat follow auxospore ‘germina- r tion’ (see p. 64). The spines that occur on the where b is the number of beads. Superficially, this end cells of four-celled coenobia of the freshwa- supported observations of Smayda and Boleyn ter chlorophyte Scenedesmus quadricauda are said (1965, 1966a, b)inThalassiosira, Chaetoceros and to reduce the sinking rate relative to a spineless other chain-forming marine diatoms that sinking ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 61

Ta b l e 2.5 Comparison of measured sinking rates (ws)ofvarious freshwater plankters and the rates (ws calc) calculated from Stokes’ equation for spheres of identical volume and density

a −1 Plankter Dynamic shape ws (µms )(ws) calc ϕr References Chlorella vulgaris ± spherical – – 0.98–1.07 Oliver et al. (1981) Chlorococcum sp. ± spherical – – 1.02–1.04 Oliver et al. (1981) Cyclotella Squat cylinder – – 1.03 Oliver et al. meneghiniana (1981) ∗Stephanodiscus Squat cylinder rotula (ds = 12–14 µm) 11.5 ± 0.8 13 ± 1 1.06 From data plotted in Fig. 2.8 (ds = 24–28 µm) 27.6 ± 2.6 26 ± 2 0.94 From data plotted in Fig. 2.8 ∗Synedra acus Attenuate cylinder (MLD = 17d) 7.3 ± 1.2 29.8 4.1 Reynolds (1984a) ∗Aulacoseira subarctica (1–2 cells) Cylinder 7.4 ± 2.8 17.2 2.3 Reynolds (1984a) (7–8 cells) Attenuate 11.4 ± 4.1 50.1 4.4 Reynolds (1984a) cylinder ∗Tabellaria Stellate, 8-armed 10.3 ± 1.0 54.1 5.5 Reynolds (1984a) ﬂocculosa var colony asterionelloides ∗Asterionella formosa (4 cells) Stellate colony 5.8 ± 0.2 18.2 3.2 Reynolds (1984a) (8 cells) Stellate colony 7.3 ± 0.6 28.9 3.9 From data plotted in Fig. 2.14 (16 cells) Stellate colony 10.7 ± 1.2 45.9 4.3 Reynolds (1984a) (8 very short Chain of ovoids 4.0 ± 0.6 7.4–8.0 1.9 Jaworski et al. cells) (1988) ∗Fragilaria crotonensis (single cell) Cylinder 3.9 ± 0.2 10.6 2.8 Reynolds (1984a) (11–12 cells) Plate 11.2 ± 0.5 54.1 4.8 Reynolds (1984a) aAsterisks indicate experiments on diatones killed prior to measurement of sinking rates, to overcome vital interference (see Section 2.5.4). 62 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

rates increasewithincreasingchainlength.How- ever, Walsby and Reynolds (1980)argued that the linear expression is misleading as increasing chain length should tend to a ﬁnite maximum. The sinking velocity of the chain (say wc) is linked to the sinking rate of the sphere of similar volume (ws), through wc = ws/ϕr.According 2 to Stokes’ equation (2.16), ws ∝ (ds/2) , where ds is the diameter of the equivalent sphere. How- 0.33 0.67 ever, ds/2 ∝ b ,sows ∝ b ,i.e.ws does not increase linearly, as Hutchinson’s equation predicts, neither does it fall asymptotically to zero as implied.

Cylinder elongation and cylindrical filaments This theory is upheld by the data of another set of observations presented by Reynolds (1984a)for filaments of Melosira italica (now Aulacoseira subarctica). This freshwater diatom comprises cylindrical cells joined together by the valve ends, effectively lengthening the cylinder in a linear way. In Reynolds’ experiments, the mean length of the cells was hc = 19.0 µm, the mean diameter (dc) Figure 2.11 Plot of sinking rates (w ) against length (as was 6.3 µm. The external volume of the cylindical s cells per filament) of Aulacoseira subarctica filaments compared cell was calculated from π(d /2)2 h ∼592 µm3. c c with the sinking rates calculated for a spheres of the same The ratio h /d ,asortofindex of cylindricity, c c volume and density (ws calc). The ratio, φr = (ws calc)/ws,is is 3.0 and the diameter of the sphere (ds)ofthe also shown against the horizontal axis. Redrawn from same volume is ∼10.4 µm. Adding another cell Reynolds (1984a) doubles the length, volume and cylindricity, but thearea of mutual contact between them means that the surface is not quite doubled but the (200–220 µm, hc/dc ∼ 30, ϕr ∼ 4.5). This velocity diameter of the equivalent sphere is increased is, moreover, about the same as that calculated by about a third, to 13.1 µm. The sinking rates forasphere of similar density and of diameter (ws)ofindividual filaments of a killed suspen- equivalent to only 1.2 cells. Thus, the sacrifice of sion of an otherwise healthy, late-exponential extra sinking speed is small in relation to the strain of Aulacoseira (excess density ∼251 kg m−3) gain in size and where the loss of surface area is were measured directly and grouped according probably insignificant. to thenumber of cells in the filament. The mea- It is, of course, a feature of many pennate surements were compared directly with the rates diatoms in the plankton to have finely cylin- calculated for spheres of equivalent volume and drical cells. On the basis of a small number excess density (ws calc) in Fig. 2.11;equivalent val- of measurements on a species of Synedra and ues of ϕr (as ws calc/ws)arealsoincluded. treating the essentially cuboidal cells as cylin- The plot is instructive in several ways. Length- ders (hc = 128±11 µm, greatest dc ∼ 8.9 µm, ening increases size as it does ws.Filament forma- hc/dc 13–16), Reynolds (1984a)solved ϕr (as ws tion does not decrease sinking rate with respect calc/ws) ∼ 4.1. For the shorter individual cuboidal to single cells. On the other hand, the increments cells of Fragilaria crotonensis, whose length become smaller with each cell added, with an (∼70 µm) exceeded mean width (3.4 µm) byafac- −1 asymptote (in this instance) of about 15 µms , tor ofover20, ϕr wasdetermined to be about 2.75. reached by a filament of 11–12 cells in length In the experiments with single cells of Asterionella ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 63

sured sinking rates of killed coenobia of Fragi- laria crotonensis are plotted against the numbers of cells in the colonies and compared with the curve of (ws calc) predicted for spheres of the same volumes. Whereas, once again, Stokes’ equation predicts a continuous increase in sinking rate against size, coenobial lengthening tends to stability at 16–20 cells, not far from the point, indeed, at which the lateral expanse exceeds thelengths of the component cells and the coenobium starts to become ribbon-like. It is not unusual to encounter ribbons of Fragilaria in nature exceeding 150 or 200 cells (i.e. some 500–700 µminlength) but it is perhaps initially surprising to find that they sink no faster than filaments one-tenth their length! A further tendency that is only evident in these long chains is that the ribbons are not always flat but are sometimes twisted, with a frequency of between 140 and 200 cells per complete spiral. The extent to which this secondary structure influences sinking behaviour is not known. The secondary shape of Asterionella coenobia is reminiscent of spokes in a rimless wheel, set generally at nearly 45◦ to each other. When there are eight such cells, they present a handsome star Figure 2.12 Plot of sinking rates (ws) against the number of shape (alluded to in the generic name), although cells of killed Fragilaria crotonensis colonies compared with the the mutual attachments determine that the sinking rates calculated for a sphere of the same volume and colony is not flat but is like a shallow spiral φ = / density (ws calc). The ratio, r (ws calc) ws,isalso shown staircase. Cell no. 9 starts a second layer; in cul- against the horizontal axis. Redrawn from Reynolds (1984a). tures and in fast-growing natural populations, coenobia of more than eight cells are frequently formosa (length 66 µm, mean width 3.5 µm) the observed (although, in the author’s experience, form resistance was found to fall in the range chains of over 20–24 cells are in the ‘rare’ cate- 2.3 to 2.8. Compared with the squat cylindri- gory). Following a similar approach to that used cal shapes of the centric diatoms Cyclotella and for Aulacoseira and Fragilaria,Reynolds (1984a) Stephanodiscus species for which measurements plotted measured sinking rates of killed coenobia are available, the impact of attenuation on form against the numbers of cells in the colony and, resistance is plainly evident (see Table 2.5). again, compared them with corresponding curve (ws calc) for spheres of the same volumes (see Colony formation Fig. 2.13). Now, although the observed sinking Of course, both Fragilaria and Asterionella are rates, ws,suggest the same tendency to be asymp- more familiarly recognised as coenobial algae, totic up to a point where there are 6–10 cells in thecells in either case remaining tenuously the coenobium, it is equally clear that higher attached on the valve surfaces, in the central numbers of cells make the colony sink faster, region in Fragilaria (to form a sort of double-sided with no further gain in ϕr after ∼4.0. Reynolds comb) and at the flared, distal end in Asterionella. (1984a)interpreted this result as demonstrating These distinctive new shapes generate some the advantage to form resistance of creating a interesting sinking properties. In Fig. 2.12,mea- new shape, from a cylinder to a spoked disc, 64 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

study of Asterionella,using different source material, but its results fitted comfortably into the pattern. As pointed out earlier, several separate studies of the sinking rates of typical, eight-celled colonies of Asterionella,usingquite disparate sources of algae, having differing dimensions and, possibly, densities, nevertheless achieved strikingly similar results (generally ws = 5.5–11.0 µms−1), provided that the material used was moribund, poisoned or killed prior to measurement. However, the clearest demonstration that the sinking characteristics are strongly governed by shape comes from the somewhat fortuitous experimentation opportunity presented to Jaworski et al.(1988). When diatoms grow and divide, the replication of the siliceous cell wall is achieved by the development of a ‘new’ valve inside each of the two mother valves. When the daughters are eventually differentiated as new, independent entities, one has the dimensions of its parent cell but the other is slightly smaller, being no larger than the smaller of the parental valves (Volcani, 1981;LiandVolcani, 1984;Craw- Figure 2.13 Plot of sinking rates (ws)ofkilled stellate ford and Schmid, 1986). In a clone of succes- colonies of Asterionella formosa of comprising varying numbers sive generations, one cell retains the parental of cells, compared with the sinking rates calculated for a dimensions but all the others are, to varying spheres of the same volume and density (w calc). The ratio, s extents, smaller. Average size must diminish in φr = (ws calc)/ws is also shown against the horizontal axis. Redrawn from Reynolds (1984a). proportion to the number of divisions. This is clearly not a process without limit, as the species- specific sizes of diatoms normally remain within which however is lost if space between cells is stable and predictable limits. Size is recovered progressively plugged by more, dense cells that periodically through distinctive auxospore stages, add nothing to the hydrodynamic resistance. which give rise to vegetative cells, with relatively It is a satisfying piece of teleology that the large overall dimensions and large sap vacuoles. maximum advantage should seem to be achieved This process is observed in culture as well as in at the most typical coenobial size. Indeed, there nature. When it was noticed, however, that sub- is further observational and experimental evi- cultured cells of Asterionella clone L354, one of dence that the shape determines more of the those isolated from wild types and maintained sinking behaviour of stellate colonies than any at the Ferry House Laboratory of the Freshwater of the Stokesian components. First, the argu- Biological Association, were becoming unusually ment would need to hold for Tabellaria flocculosa small, it was decided to include it in the sinking var. asterionelloides, whose robust cells form eight- studies that were then being conducted in the armed stellate colonies that contrast with the laboratory. These observations were commenced more typical habits adopted by this genus (see in 1981 and were continued until 1986 (Jaworski Knudsen, 1953). Frequently, up to 16 cells com- et al., 1988). The clone never did recover size prise the colonies but they remain in adherent but the rate of growth became extremely slow pairs, preserving a regular eight-radiate form. towardsthe end. By the time of the last measure- It is also of significance that some of the ments, late in 1985, the cells had shrunk from entries in Fig. 2.13 were derived from another long cuboids, 65 µminlength,tostubby ovoids, ADAPTIVE AND EVOLUTIONARY MECHANISMS FOR REGULATING WS 65

against colony volume and compared with ws calc of equivalent spheres having the same densities. As the size of the cells diminished over thefirst 2 years (during which time the mean colony volume reduced by nearly two-thirds and themean density difference with the medium almost doubled), sinking rates actually increased slightly. The rising mean of about 7.2 to one of 8.0 µms−1 does not violate the hypothesis that the stellate cell arrangement dominates the sinking rate. Thereafter, with the aggregate volumes of colonies below 1200 µm3,sinking rate diminished. The curve fitted to all sinking rate determinations (curve 1 in Fig. 2.14)revealslessof what is happening than do the two separate fitted curves referring to colonies >1200 µm3 (curve 2) and those <1200 µm3 (curve 3). By taking each of these regression lines and using them to solve form resistance as the calculated sinking rate for a sphere divided by the regression- predicted actual sinking rate, the relationship is further amplified. Curve (4) for all points (corresponding to regression 1) shows the typical form-resistance outline, albeit rather flattened. The right-hand side of curve 5, corresponding to regression 2, quickly takes ϕr > 2and> 3, towards the ‘plateau’ level shown in Fig. 2.13. To theleft of curve 5 (corresponding to regres- Figure 2.14 Plot of sinking rates of killed, stellate sion 3), sinking rate varies more closely with vol- eight-celled colonies of Asterionella cells of diminuitive length ume (though not so steeply as ws calc); ϕr is in and volume, compared with the sinking rates calculated for a therange 1.6–2.4. The change in behaviour has sphere of the same volume and density (ws calc). Three apivot point when the colony falls below 1200 regressions are fitted to the observed values: (1) applies to all µm3, when individual cell volumes are <150 µm3 > µ 3 points, (2) to those colonies 1000 m in volume and (3) and the cells are 18–20 µminlength. The likely to those <1000 µm3 in volume. The ratio, φ = (w calc)/w r s s significance of this is that the hydromechanical is shown against the horizontal axis with respect to the characteristics of the star shape are eventually estimates of ws derived from regression equation (2.1) (curve 4) and those combining equations (2.2) and (2.3) (curve 5). overtaken bythoseofagyre of ovoids, more rem- Redrawn with permission, from Jaworski et al.(1988). iniscent ofAnabaena than Asterionella. Some of these measurements are included in the summaries of calculated form resistance measuring about 5.5 µmwithabasal width of owing to shape distortions. 4.2 µmandaheight of 2.1 µm. Significantly, the cells maintained mutual connections and there 2.5.4 Vital regulation of sinking rate remained plenty of eight-armed colonies in the We may return, briefly, to the ability of live culture. The dry mass of cells and the silica con- phytoplankton, especially diatoms, to exercise tent of the walls diminished with size but overall this further control on their own sinking rates density increased (from ∼1100 to 1200 kg m−3). below that expected from a modified Stokes equa- The sinking rates (ws)ofkilledcells measured tion, with all components properly evaluated. It over the five year period are plotted in Fig. 2.14 has to be confirmed first that we use a correct 66 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

interpretation of facts. Smayda (1970)referredto varies interspecifically. It is not known whether the acceleration of sinking rates in moribund theform of the valves responds to environmen- diatoms, and the several mechanisms by which tal control, so making it possible to build longer this might come about. These include the aggre- chains and filaments or shorter ones, according gation of dying cells and, through their involve- to circumstances. Many papers refer to varying ment with other planktic detritus (zooplankton numbers of cells per coenobium during growth exuviae and faecal fragments, colloidal organ- and senescence, perhaps speculating on the role ics, fragments of plant remains), their forma- of nutrient limitation. Observations on many nat- tion in to larger floccular particles, collectively ural populations and of isolates treated in the known as ‘marine snow’ (Alldredge and Silver, laboratory leads me to the view that coenobia are 1988). In these aggregates, particles may sink larger (i.e. comprise more cells) if grown rapidly faster than might be predicted if they were sepa- in unshaken cultures but are more fragmented in rated. However, the consistency and reproducibil- old cultures, with many moribund cells. These ity of behaviour of killed cells having similar clearly make some impact on sinking rate but, form resistance should prompt us to regard this as we have shown already, these are relatively as the ‘normal’ sinking performance and to ask small compared to the sinking-rate variations how it might be that live, healthy cells reduce attributable to changes in the physiological vital- their sinking rates below those that Stokes’ law ity of the cells. would predict. The physiological mechanisms regulating The scale of these reductions is impressive, sinking rate remain stubbornly resistant to expla- the ‘live’ rate being up to one order of magni- nation. Over a number of years, colleagues at tude, and frequently two- to four-fold less than theFerry House supported my efforts to develop the ‘killed’ rate. As well as the case of Stephano- aplausible hypothesis for this behaviour. It is discus rotula illustrated in Fig. 2.8,thereis an not an entirely negative outcome to say that abundance of data to show the sinking rates of these succeeded only in excluding several pos- healthy, eight-celled Asterionella formosa colonies sibilities. We never found a sufficient or suffi- to be typically 2–3 µms−1 (about 0.2–0.3 m d−1) ciently responsive variation in density that would rather than the 7–8 µms−1 explained by the explain a two- or three-fold change in sinking modified Stokes’ equation (Smayda, 1974;Tilman rate. While we were able to bring pressure to bear and Kilham, 1976;Jaworski et al., 1981;Wise- on planktic Cyanobacteria to collapse gas vesi- man and Reynolds, 1981). Similarly, variations in cles, to subject diatoms to similar treatment – up the sinking rate of Fragilaria crotonensis may be to about 12 bars, anyway – produced no response <0.4 m d−1 for long periods but quite quickly at all. Yet if sufficient of the specific photosyn- increase to up to 1.1 m d−1 (≤13 µms−1) when thetic inhibitor DCMU [3-(3,4-dichlorophenyl)-1,1- cells are nutrient limited or have been exposed dimethyl urea] is added to a healthy, slow-sinking to excessive sunlight (Reynolds, 1973a, 1983a). suspension of Asterionella cells to block their pho- Indeed, these studies have suggested that it is tosynthesis, sinking rate rose quickly to the rates auseful biological adaptation for an otherwise of killed or moribund examples. In time, both non-motile organism to be able to increase sink- effects are reversible (photosynthetic capacity, ing rate spontaneously and to ‘accelerate out of sinking-rate control are recovered). Contempor- danger’ from excessive irradiance, especially in aneous work in our laboratory on the susceptibil- stabilising water columns (Reynolds et al., 1986). ity of Asterionella formosa to attack by parasitic It might appear that regulation of sinking fungi (see especially Canter and Jaworski, 1981) rate is under the control of the diatom. Certainly, had just revealed that, under conditions of low variability in the number of cells per colony may light or darkness, infective chytrid zoospores are be, to an extent, self-regulated as the intercellular not attracted to Asterionella cells as they are in links vary in structure, some being much more thelight. We deduced that actively photosynthe- amenable to separation than others. The fre- sising cells either broadcast a signal to the adja- quency of ‘linking valves’ and ‘separation valves’ cent medium advertising their presence or that SINKING AND ENTRAINMENT IN NATURAL TURBULENCE 67 they create a local change in the medium that is that it might be trailed in threads from cells, exploited or avoided by the infective spores. The like a parachute or in the manner of the chitin lateral thinking that arose from our discussions hairs of Thalassiosira.Unlike chitin, threads of led to the hypothesis that photosynthesising cells mucilage require active maintenance by healthy were immobilising water around their periphery. cells but would be sufficiently frail to be shed Thus, the particle acquires a new identity and quickly, when they become a liability or too costly the new dimensions of alga + water, in much to maintain. Traditional algal anatomists would the similar way that an investment of mucilage concur in conversation that such mucilaginous provides (see Section 2.5.2). threads and trails exist but there seems very little Considering that a sufficient swathe of published to uphold a compelling case. Even the mucilage has not been observed in these algae, use of Indian-ink irrigation, a popular technique the candidate mechanism that we proposed was forrevealing mucilaginous structures, has proved that the surface charge on the cells was variable unhelpful to the argument. However, a recent and that this might affect the amount of water description of mucilaginous protuberances radi- thus immobilised. This was not an original inspi- ating from the marginal cells of Pediastrum duplex ration but an echo of an earlier hypothesis, put colonies (Krienitz, 1990) has been confirmed in forward by Margalef (1957). Based on his own thephotomicrographs of Padisak´ et al.(2003a). observations of differing polarity and electro- Back in the 1980s, we had proposed a num- kinetic (‘zeta’) potential of Scenedesmus cells, he ber of approaches to investigate the hypothe- developed a theory of ‘structural viscosity’, where sis, including the possibility of using WETSTEM algae regulated the viscosity of their immedi- electron microscopy, for the observation of liv- ate surroundings through the electrical charge ing materials at high magnification, which was on the outer cell wall. It must be emphasised then just becoming available. However, this was that, like any other small particles dispersed in also the time when the sponsorship of science an electrolyte (albeit, a very weak one), algae wasmoving rapidly from academic, curiosity-led carry a surface charge in any case. This is, in problems such as this. Purchase or lease of suit- part, determined by the ionic strength of the able apparatus was less the problem than was the medium. Moreover, several publications detail- continued support to sustain an active group of ing direct measurements of surface charge using personnel. Resolution of the mechanism of vital electrophoretic procedures were available (Ives, regulation of sinking rate by diatoms remains 1956;Grunberg,¨ 1968;Hegewald, 1972;Zhurav- open to future research. leva and Matsekevich, 1974). It became our objective to demonstrate that variable sinking rates are related to physiologically mediated changes 2.6 Sinking and entrainment in in surface charge. We used an electrophore- sis microscope to determine simultaneously the natural turbulence sinking rates and electrophoretic mobility of Aste- rionella colonies, incubated under varying labora- 2.6.1 Sinking, floating and entrainment tory conditions (Wiseman and Reynolds, 1981). Preceding sections of this chapter have reviewed The outcome was quite clear, insofar as large thescales of the quantities of the two key com- changes in sinking rate could not be correlated ponents of plankton entrainability – the veloci- with relatively small variations in surface charge. ties of the intrinsic tendency of plankton to sink, The experiments succeeded only in rejecting swim or float and the velocities of motion in another hypothesis about sinking-rate regulation themedium. Both typically cover several orders and in establishing a nice method for the direct of magnitude. The sinking rates of diatoms measurement of sinking rates. span something like 1 µms−1 to 6 mm s−1. The (as yet) unexplored alternative hypothesis The flotation rates of buoyant colonies of the we put forward (Wiseman and Reynolds, 1981) Cyanobacteria such as Anabaena and Aphani- referred to a quite different role for mucilage, zomenon may reach 40–60 µms−1,typical colonies 68 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Figure 2.15 Ranges of sinking (‘DOWN’) and floating (‘UP’) velocities of freshwater phytoplankters, or, where appropriate of vertical swimming rates of motile species, plotted against unit volume. The algae are: An flo, Anabaena flos-aquae; Aphan, Aphanizomenon flos-aquae; Ast, Asterionella formosa; Aul, Aulacoseira subarctica; Cer h, Ceratium hirundinella; Chlm, Chlorococcum; Chlo, Chlorella; Clo ac, Closterium aciculare; Cycl, Cyclotella meneghiniana; Fra c, Fragilaria crotonensis; Mic; Microcystis aeruginosa; Pla ag, Planktothrix agardhii; Sta p, Staurastrum pingue; Ste r, Stephanodiscus rotula; Volv, Volvox aureus. Redrawn with permission from Reynolds (1997a).

of Gloeotrichia and Microcystis may achieve 100–300 suspension. Larger species potentially move faster µms−1, while some of the largest aggregations or farther but they need to be either flagellate achieve 3–4 mm s−1 (Reynolds et al., 1987;Oliver, or to govern their own buoyancy to counter the 1994). Among motile organisms, reported ‘swim- tendency to sink. Indeed, thereisastrongindi- ming speeds’ range between 3–30 µms−1 for the cation that their ability to overcome elimination nanoplanktic flagellates to 200–500 µms−1 for from the plankton, at least in the extant vege- thelarger dinoflagellates, such as freshwater Cer- tative stages of their life cycles, depends upon atium and Peridinium (Talling, 1971;Pollingher, theamplification of motility that large size con- 1988)andmarine Gymnodinium catenatum and Lin- fers. In essence, phytoplankton motility can be gulodinium spp. (see Smayda, 2002). Large colonies differentiated among those that can do little to of Volvox can attain almost 1 mm s−1 (Sommer stop themselves from sinking (mostly diatoms), and Gliwicz, 1986) while the ciliate Mesodinium thevery large, which self-regulate their move- is reported to have a maximum swimming speed ments, and the very small for which it seems to of 8 mm s−1 (Crawford and Lindholm, 1997). matter rather little. At theother end of the motility spectrum, Even so, when the comparison is made, the solitary bacteria and picoplankters probably sink range of intrinsic rates of sinking (ws), float- −1 no faster than 0.01–0.02 µms (data collected ing (−ws)and flagellar self-propulsion (us)rep- in Reynolds, 1987a). The data plotted in Fig. 2.15 resented in Fig. 2.15 (mostly ≤10−3 ms−1)are show that, despite the compounding of several 1–6 orders of magnitude smaller than the sam- factors in the modified Stokes equation (2.16), ple turbulent velocities cited in Table 2.2 (mostly the intrinsic rates at which phytoplankton move ≥10−2 ms−1). Generally speaking, the deduction ∗ (or potentially move) in relation to the adjacent is that ws u . This does not mean that the sink- medium are powerfully related to their sizes. ing potential (or the floating or migratory poten- Smaller algae sink or ‘swim’ so slowly that the tial) is overcome, just that gravitating plankters motion of the water is supposed to keep them in are constantly being redistributed. What really SINKING AND ENTRAINMENT IN NATURAL TURBULENCE 69 matters to sinking particles is the relative magnitudes of ws and the upward thrusts of the turbulent eddies w (see Section 2.3.1). If ws > w ,nothing prevents the particle from sinking. While, however, ws < w some particles can be transported upwards faster than they gravitate downwards–andtheirsinking trajectories are reiniti- ated at a higher point in the turbulence field. Of course, there are, other things being equal, downward eddy thrusts which add to rate of vertical descent of the particles. Given that the upward and downward values of w are self-cancelling, ws is not affected. However, the greater is the magnitude of w relative to ws,themoredominant is the redistribution and the more delayed is the descent of the particles. In this way, the ability of fluid turbulence to Figure 2.16 The entrainment criterion, as expressed in Eq. (2.19). In essence, the larger is the alga and the greater its maintain sinking particles in apparent suspen- intrinsic settling (or flotation) velocity, then the greater is the sion depends on the ratio ofsinking speed to the turbulent intensity required to entrain it. Redrawn with vertical turbulent velocity fluctuations. Empiri- permission from Reynolds (1997a). cal judgement suggested that this entrainment threshold occurs at 1–2 orders of magnitude greater than the intrinsic motion of the par- and oceans, u∗ is a highly variable quantity (see, ticle. In a detailed consideration of this rela- e.g., Table 2.2), with the variability being often tionship, Humphries and Imberger (1982)intro- expressed over high temporal frequencies (from duced a quotient (herein referred to as )to theorder of a few minutes) and, sometimes, over represent the boundary between behaviour domi- quite short spatial scales. Whilst in near-surface nated by turbulent diffusivity of the medium and layers even the lower values u∗ may often still be behaviour dominated by particle buoyancy: an order of magnitude greater than the intrin- / sic particle properties, the entrainment condi- = w /15[(w )2]1 2 (2.19) s tion is not necessarily continuous in the vertical Noting that, in open turbulence, the magnitude direction. Just taking the example of the transfer of u∗ is not dissimilar from [(w)2]1/2 (see Eq. (2.4)), of the momentum of wind stress on the water Reynolds (1994a)proposed that substitution of surface and the propagation of turbulent eddies u∗ in Eq. (2.19)gaveauseful approximation to in the water column below (Eq. 2.5), it is clear the value of . The main line drawn into Fig. that the loss of velocity through the spectrum 2.16 ( = 1) against axes representing sinking of diminishing eddies will continue downwards ∗ rate (ws)andturbulent velocity (u ), is proposed into the water to the point where the residual as the boundary between effective entrainment energy is overcome by viscosity. As the penetrat- (diffusivity dominates distribution) and effective ing turbulence decays with depth, the entraining disentrainment (particle properties dominate dis- capacity steadily weakens towards a point where tribution). neither u∗ nor [(w)2]1/2 can any longer satisfy the The adjective ‘effective’ is important, because particle-entrainment condition. In other words, entrainment is never complete while ws has finite the turbulence field is finite in extent and is open value; neither is disentrainment total while there to theloss of sedimenting particles (and, equally, is any possibility that motion in the water can to the recruitment of buoyant ones). deflect the particle from its intrinsic vertical This leads us to a significant deduction about trajectory. However, the main point requiring thesuspension and continued entrainment of emphasis at this point is that, in lakes, rivers phytoplankton in lakes and the sea. It is the extent 70 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

of the turbulence, rather than its quantitative number remaining in the column (Nt)isapprox- magnitude, that most influences the persistence imately or otherwise of various types of organism in the N = N (1 − w t/h ) (2.20) plankton. For the same reason, the factors that t 0 s w influence the depth of the turbulent mixed layer Let us suppose that the column is now instan- and its variability are important in the survival, taneously and homogeneously mixed, such that seasonality and succession of phytoplankton in the particles still in the column are redistributed natural waters. These are reviewed briefly in later throughout the column but those that have sections but it is first necessary to consider their already settled into the basal boundary layer are behaviour within the mixed layer itself. not resuspended. This action reintroduces particles (albeit now more dilute) to the top of the column and they recommence their downward 2.6.2 Loss of sinking particles from trajectory. Obviously, the time to complete set- turbulent layers tling is now longer than t (though not longer The purpose of this section is not to demonstrate than 2t). that sinking particles are lost from turbulent, The process could be repeated, each time leav- surface-mixed layers but to provide the basis of ing the settled particles undisturbed but redis- estimating the rate of loss. The converse, how tributing the unsettled particles on each occa- slowly they are lost, is the essence of adapta- sion. If, within the original period, t, m such tion to planktic survival. The development here mixings are accommodated at regular intervals, is rather briefer than that in Reynolds (1984a), as separating quiescent periods each t/m in dura- its principles are now broadly accepted by plank- tion. The general formula for the population ton scientists. Its physical basis is rather older, remaining in suspension after the first short owing to Dobbins (1944)andCordoba-Molina et period is derived from Eq. (2.20): al.(1978). Smith (1982) considered its application N / = N (1 − w t /mh ) (2.21) to plankton. Interestingly, empirical validation of t m 0 s w the theory comes from using plankton algae in After the second, it will be laboratory-scale measurements. N (1 − w t /mh )(1 − w t /mh ) Let us first take the example of a completely 0 s w s w static water column, of height hw (in m), open and after the mth, at the surface with a smooth bottom, to which m N = N (1 − w t /mh ) (2.22) small inert, uniform particles are added at the t 0 s w top. Supposing their density exceeds that of the Because t = hw/ws, Eq. (2.22)simplifies to water, that they satisfy the laminar-flow condi- m N = N (1 − 1/m) (2.23) tion of the Stokes equation and sink through t 0 the water column at a predictable velocity, ws (in As m becomes large, the series tends to an expo- ms−1), then the time they take to settle out from nential decay curve the column is t = hw/ws (in s). If a large num- = / −3 Nt N0(1 e) (2.24) ber (N0,m )ofsuchparticles are initially distributed uniformly through the water column, where e is the base of natural logarithms (∼2.72). after which its static condition is immediately Solving empirically, restored, they would settle out at the same rates N = 0.368 N (2.25) but, depending on the distance to be travelled, t 0 in times ranging from zero to t. The last particle This derivation is instructive in several respects. will not settle in a time significantly less than The literal interpretation of Eq. (2.25)isthat t, which continues to represent the minimum repeated (i.e. continuous) mixing of a layer period in which the column is cleared of parti- should be expected still to retain 36.8% of an ini- cles. At any intermediate time, t,theproportion tial population of sinking particles at the end of particles settled is given by N0 ws t/hw. The of a period during which particles would have SINKING AND ENTRAINMENT IN NATURAL TURBULENCE 71

Figure 2.17 The number of particles retained in a continuously mixed supension compared to the retention of the same particles in a static water column of identical height. Redrawn from Reynolds (1984a).

left the same layer had it been unmixed. More- phytoplankton, because mixed layers may range over, the time to achieve total elimination (te)is from hundreds of metres in depth down to few an asymptote to inﬁnity but we may deduce that millimetres and, in any given water body, the the time toachieve95% or 99% elimination is variability in mixed-layer depth may occur on (respectively) calculable from timescales of as little as minutes to hours.

te/t = log e0.05/log 0.368 = 3.0 2.6.3 Mixed depth variability in natural or water columns Turbulent extent defines the vertical and hori- t /t = log 0.01/log 0.368 = 4.6 e e zontal displacement of particles that fulfil the Using this approach, the longevity of suspension entrainment criterion (Fig. 2.16). The vertical can be plotted (Fig. 2.17). It takes three times extent of turbulent boundary layers, uncon- longer for 95% of particles to escape a mixed layer strained by the basin morphometry or by than were the same depth of water left unmixed. thepresence of density gradients (open turbu- It may also be noted that the number of mixings lence), is related primarily to the kinetic energy does not havetobevasttoachievethiseffect. transferred: rearranging Eq. (2.9), Substituting in Eq. (2.23), if m = 2, Nt = 0.25 N0; ≈ ∗ / −1 if m = 5, Nt = 0.33 N0;ifm = 20, Nt = 0.36 N0. le (u )(du dz) m (2.26) The formulation does not predict the value of the basetime, t.However, it is abundantly where (du/dz)isthe vertical gradient of horizon- −1 −1 evident from the rest of this chapter that, the tal velocities (in m s m )andle is the dimen- smaller is the specific sinking rate, ws,thelonger sion of the largest eddies. Entries in Table 2.2 per- will be t for any given column of length, hm.Fur- taining to the upper layers of the open ocean and ther, the greater isthemixeddepth,thenthe also of a moderately large lake like the Bodensee longer is the period of maintenance. Any ten- (Germany/Switzerland) imply an increase in mix- dency towards truncation of the mixed depth, ing depth of about 9 m for each increment in −1 hm,will accelerate the loss rate of any species wind forcing of 1 m s .Ofcourse, even this rela- that does not have, or can effect, an absolutely tionship applies only under a constant wind: slow rate of sinking. an increase in wind speed necessarily invokes a This confirms the adaptive significance of a restructuring, which may take many minutes to slow intrinsic sinking rate. It has much less to organise (see below). Similarly, the contraction do with delaying settlement directly but, rather, of the thickness of the mixed layer following a through the extension it confers to average res- weakening of the wind stress is gradual, pending idence time within an actively-mixed, entrain- thedissipation of inertia. The structure of turbu- ing water layer. The relationship also provides lence under a variable, gusting wind is extremely amajor variable in the population ecology of complex! 72 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

The complexity is further magnified in small still water (such as at night), the heat trans- basins (Imberger and Ivey, 1991;Wuest¨ and Lorke, ferincreases the density of the surface water 2003). Where the physical depth of the basin con- and causes instability. The denser water is liable strains eventhisdegreeofdissipative order, the to tumble through the water column, acceler- water is fully mixed by a turbulence field which ating as it does so and displacing lighter water is, as already argued, made up by a finer grain of upwards, until it reaches a depth of approximate eddies. Moreover, the shallower is the water body, isopycny (that is, where water has the identical the lower is the wind speed representing the density). This process can continue so long as the onset of full basin mixing likely to be. Thus, from heat imbalance between air and water persists, the entries in Table 2.2,itispossible to deduce all the time depressing the depth of the density that a wind of 3.5 m s−1 might be sufficient to gradient. The energy of this penetrative convection mix Lough Neagh, Northern Ireland (maximum may be expressed: depth 31 m, mean depth 8.9 m). In fact, the lake B = (gγ Q ∗)(ρ σ )−1 Wm2 s−2 J−1 (= m2 s−3) is usually well mixed by wind and is often quite Q T w turbid with particles entrained by direct shear (2.28) stress on thesediment. At all other times, the buoyancy acquired by Density gradients, especially those due to the thewarmer water resists its downward trans- thermal expansion of the near-surface water sub- port through propagating eddies, whether gener- ject to solar heating, also provide a significant ated by internal convection or externally, such as barrier to the vertical dissipation of the kinetic through the work of wind. They are instead con- energy of mixing. Although there is some out- fined to a layer of lesser thickness. Its depth, h , ward conduction of heat from the interior of b tends to a point at which the kinetic energy ( J ) the Earth and some heatisreleasedinthedis- k and buoyancy ( J )forces are balanced. Its instan- sipation of mechanical energy, over 99% of the b taneous value, also known as the Monin–Obukhov heat received by most water bodies comes directly length, may be calculated, considering that the from the Sun. The solar flux influences the ecol- − kinetic energy flux, in W m 2,isgivenby: ogy of phytoplankton in a number of ways but, ∗ ∗ 3 −3 in the present context, our concern is solely the J k = τ(u ) = ρw(u ) kg s (2.29) direct role of surface heat exchanges upon the vertical extent of the surface boundary layer. while the buoyancy flux is the product of the Starting with the case when there is no wind expansion due to the net heat flux to the water ∗ −2 and solar heating brings expansion and decreas- (Q T), also in W m , ◦ ing water density (i.e. its temperature is >4 C), a = / γ ∗ · σ −1 −3 J b 1 2ghb Q T kg s (2.30) positive heat flux is attenuated beneath the water surface so that the heating is confined to a nar- where γ is the temperature-dependent coefficient row near-surface layer. The heat reaching a depth, of thermal expansion of water, σ is its specific −1 −1 z,isexpressed: heat (4186 J kg K ) and g is gravitational acceleration (9.8081 m s−2). ∗ −kz −2 Q z = Q e Wm (2.27) T Then, when J b = J k,

where e is the base of natural logarithms and ∗ 3 ∗ −1 hb = 2σρw(u ) (gγ Q ) m (2.31) k is an exponential coefficient of heat absorp- T ∗ tion. Q T is that fraction of the net heat flux, Q T Owing to the organisational lags and the vari- which penetrates beyond the top millimeter or ability in the opposing energy sources, Eq. (2.29) ∗ so. Roughly, Q T averages about half the incoming should be considered more illustrative than pre- short-wave radiation, Q S. The effect of acquired dictive. Nevertheless, simulations that recognise buoyancy suppresses the downward transport of the complexity of the heat exchanges across the heat, save by conduction. surface can give close approximations to actual If the water temperature is <4 ◦C, or if it events, both over the day (Imberger, 1985)and is > 4 ◦Cbuttheheatflux is away from the over seasons (Marti and Imboden, 1986). SINKING AND ENTRAINMENT IN NATURAL TURBULENCE 73

The effect of wind is to distribute the heat evenly throughout its depth, hm.Iftheheat ﬂux across its lower boundary is due only to conduction and negligible, the rate of temperature change of the whole mixed layer can be approximated from the net heat ﬂux,

θ/ = ∗ ρ σ −1 −1 d dt Q T(hm w ) Ks (2.32)

The extent of the turbulent mixed boundary layer may be then viewed as the outcome of a continuous ‘war’ between the buoyancy generating forces and the dissipative forces. The battles favour one or other of the opponents, ∗ depending mostly upon the heat income, Q T, and the kinetic energy input, τ,asencapsu- lated in the Monin–Obukhov equation (2.31). Note that if the instantaneous calculation of hb is less than the lagged, observable hm,buoyancy forces are dominant and the system will become more stable. If hb > hm, turbulence is dominant and the mixed layer should be expected to deepen. It becomes easy to appreciate how, at least inwarmclimates,whenthewatertem- peratures are above 20 ◦Cforsustained periods, diurnal stratification and shrinkage of the mixed depth occurs during the morning and net cooling leads to its breakdown and extension of the mixed depth during the afternoon or evening. The example in Fig. 2.18 shows the outcome of diel fluctuations in heat- and mechanical-energy fluxes to the density structure of an Australian reservoir.

2.6.4 Vertical structure in the pelagic Over periods of days of strong heating and/or weak winds, during which convective energy is insufficient to bring about complete overnight Figure 2.18 Diel variability in the mixed depth of a subtropical reservoir (Wellington Reservoir, Western mixing, there will develop a residual density dif- Australia), reflecting the net heat exchanges with the ference between the surface mixed layer and the atmosphere. The top panel shows the depth distribution of water beneath it, leading to the formation of isotherms through a single day. The left-hand column of amoreenduringdensity gradient, or thermo- smaller graphs shows features of the evolving temperature cline. Its resistance to mixing is acquired dur- structure (based on Imberger, 1985). The right-hand column ing preceding buoyancy phases. This resistance proposes stages in the season-long development of enduring is expressed by the (dimensionless) bulk Richard- stratification. Redrawn with permission from Reynolds (1997a). son number, Rib,expressing the ratio between the two sets of forces:

∗ 2 −1 Rib = [ρwghm][ρw(u ) ] (2.33) 74 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

where ρw is the density difference between than a few hours or days at a time (polymictic). the surface mixed layer and the water beneath It explains the patterns of seasonal stratification the thermocline. Imberger and Hamblin (1982) in tropical lakes wherein stable density struc- divided Rib by the aspect ratio (i.e. the horizon- tures are precipitated by relatively small gains tal length ofthelayer,L,by,divided by its thick- in heat content but are correspondingly liable ness, hm)inordertotesttherobustness, in any to major mixing episodes for a relatively small given system, of the density gradients detectable. drop in suface temperature (atelomictic lakes). It This (still dimensionless) ratio, they named after can be used to test the contribution of ionic another atmosphere scientist, Wedderburn. strength (e.g. salt content in reinforcing density gradients). = −1 W Rib[Lhm] Examples of all these kinds of stratification, 2 ∗ 2 −1 = [ρwg(hm) ][ρw(u ) L ] (2.34) classified by Lewis (1983), may equally be viewed from the opposite standpoint as a series describ- Working in meters, values of W > 1areheld ing variability in the extent and duration of to describe stable structures, resistant to further turbulent mixing. The intriguing consequence down-mixing and incorporation of deeper water is that the depth of the turbulent mixed layer into the surface mixed layer, without either a (hm)may remain nearly constant, when it is significant diminution in the value of ρw (e.g. the full depth of the water (H)inashallow, through convectional heat loss across the sur- wind-exposed site. In a large, deep lake, it may face) or the sharp increase in the turbulent inten- fluctuate between <1m and >100 m, insome sity, (u∗2). Structures in which W is significantly instances, within a matter of a few hours. <1are liable to modification by the next phase The Wedderburn formulation equation has of wind stress. also been used to determine whether lakes will This relationship is especially sensitive to the stratify at all. Putting W = 1 and interpolating onset of thermal stratification and, equally, simu- theobserved summer-thermocline depths of a lates the occurrence of mixing events. The insets series of temperate lakes, Reynolds (1992c)rear- in Fig. 2.18 show the onset of an early-season ranged Eq. (2.34)todetermine the density dif- thermocline, when net strong daily heating and ference, ρw, between the waters separated by theabsence of sufficient wind action or night- the seasonal thermocline. In most instances, the time convection overcome full column mixing. outcome was not less than 0.7 to 0.9 kg m−3. Aseries of days with net warming compounds At the depths of the respective thermoclines, the stability which, in acquiring increased resis- thedensity difference would resist erosion by tance, halts the downwelling mechanical energy surface-layer circulations generated by winds up at lesser and lesser depths. The stepped gradient to ∼20 m s−1.Windsmuchstronger than these of ‘fossil’ thermoclines is typical and explicable. would cause deepening of the mixed layer and It is only following a change (lesser heat income, depression of the thermocline. Interpolating the ∗ greater net heat loss or the onset of storms, W corresponding values for ρw and u ,Eq.(2.34) diminishing) that deeper penetration by turbu- was solved for hm against various nominated val- lence eats into the colder water and sharpens the ues for L. The resultant slope separated almost thermocline at the base of the mixed layer. perfectly the dataset of stratifying and non- This is the basic mechanism for the onset and stratifying lakes assembled by Gorham and Boyce eventual breakdown in temperate lakes and seas. (1989)(Fig.2.19). It also serves to track the seasonal behaviour of This outcome is a satisfying vindication of many more kinds of system other than those of theoretical modelling. Its principal virtue in middle- to high-latitude lakes. It applies to very plankton biology is to empiricise the relation- deep lakes and seas, which may remain incom- ships by which familiar environmental compo- pletely mixed (meromictic)foryearsonend.It nents govern the entrainment and transport of also covers circumstances of water bodies too plankton-sized particles and how often the vari- shallow or too wind-exposed to stratify for more ous conditions might apply. SINKING AND ENTRAINMENT IN NATURAL TURBULENCE 75

and simultaneously lowering the depth of the thermocline.

2.6.5 Mixing times The intensity of turbulence required to entrain phytoplankton covers almost 2 orders of magnitude: non-motile algae with sinking rates of ∼40 µms−1 are effectively dispersed through turbulence fields where u∗ ≤ 600 µm s−1 (Eq. 2.19), whereas u∗ > 50 mm s−1 is sufficient to disperse the least entrainable buoyant −1 plankters (ws ≥ 1mms )(see Section 2.6.1). As has already been suggested, the intensity of mixing is often less important to the alga than is Figure 2.19 Depth, H, plotted against L, the length across thevertical depth through which it is mixed. The various lakes of routinely stratifying (•) and generally depth of water through which phytoplankton unstratified lakes (◦) considered by Gorham and Boyce is randomised can be approximated from the (1989). The line corresponds to Reynolds’ (1992c)prediction Wedderburn equation (2.34). Putting W = 1and of the wind stress required to overcome a density difference u∗ ≥ 0.6 m s−1,thenumeratorisequivalentto −3 ∗ = −1 of 0.7 kg m (equivalent to u 0.025 m s ). The diamond ≥0.36 for each 1000 m of horizontal distance, symbols refer to lakes said to stratify in some years but not in L.Dividing out gravity, the product, ρ (h )2 others Redrawn with permission from Reynolds (1997a). w m solves at ∼0.037 kg m−1. This is equivalent to an average density gradient of ≥0.04 kg m−3 m−1 per This is a suitable point at which to empha- km across a lake for a 1-m mixed layer, ∼0.01 for sise an important distinction between the thick- a2-mlayer,∼0.0045 for a 3-m layer, and so on. ness ofthemixedlayerandthedepthofthe The weaker is the average density gradient, then summer thermocline. As demonstrated here, the thegreater is the depth of entrainment likely to latter really represents the transition between be. The limiting condition is the maximum pen- the upper parts of the water column (in lakes, etration of turbulent dissipation, unimpeded by the epilimnion)thatareliabletofrequentwind- density constraints. Where a density difference mixing events and the lower part that is isolated blocks the free passage of entraining turbulence, from the atmosphere and the effects of direct theeffective floor of the layer of entrainment is wind stress (the hypolimnion). The thickness of defined by a significant local steepening of the the intermediate layer (in lakes, the metalimnion) vertical density gradient. Reynolds’ (1984a) con- is defined by the steepness of the main verti- sideration of the entrainment of diatoms, mostly cal gradient of temperature (the thermocline)or having sinking rates, ws,substantially less than density (pycnocline)between the upper and lower 40 µms−1,indicated that the formation of local layers, though neither layer is necessarily uni- density gradients of >0.02 kg m−3 m−1 probably form itself. The top of the thermocline may repre- coincided with the extent of full entrainment, sent the point to which wind mixing and/or that is, in substantial agreement with the above convection last penetrated. Otherwise, the mixed averages. For the highly buoyant cyanobacterial layer is entirely dynamic, its depth and structure colonies, however, disentrainment will occur in always relating to the current or very recent (the much stronger levels of turbulence and from previous hour) balance between Jb and Jk. The mixed layers bounded by much weaker gradients. mixed layer can be well within the epilimnion Assumption of homogeneous dispersion of or its full extent. Any tendency to exceed it, how- particles fully entrained in the actively mixed ever, results in the simultaneous deepening of layer allows us to approximate the average veloc- theepilimnion, the surface circulation shearing ity of their transport and, hence, the average time off and entraining erstwhile metalimnetic water of their passage through the mixed layer. In their 76 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

elegant development of this topic, Denman and sediment traps was to have been a part of this Gargett (1983)showedthat the average time of programme and it was decided that the choice travel (tm)through a mixed layer unconstrained of traps and the authenticity of their catches by physical boundaries or density gradients cor- could be tested within the special environment responds to: of the enclosures. The plan was to add a measured quantity of alien particles to the water col- t = 0.2 h (u∗)−1 s (2.35) m m umn (actually, Lycopodium spores, well steeped in ∗ Because, in this instance, both hm and u are wetting agent and preservative), then to moni- directly scaled to the wind speed, U (Eqs. 2.5, tor the subsequent loss from suspension in the 2.11), tm is theoretically constant. Interpolation water and to compare the calculated flux with into Eq. (2.35)ofentriesinTable2.2 in respect of the sediment trap catches. Three such experi- Bodensee permit its solution at 1416 s. The proba- ments were carried out, under differing hydro- bility of a complete mixing cycle is thus 2 × 1416 graphic conditions. The results were published s(≈47 minutes). (Reynolds, 1979a)but the unexpected bonus of In the case of the wind-mixed layer of a small the experiments was the contrasting rates of loss or shallow basin, or one bounded by a den- from suspension of ostensibly identical spores sity gradient, the timescale through the layer is under the varying conditions. inversely proportional to the flux of turbulent In the first experiment, carried out in win- kinetic energy: ter, thespores were dispersed over the enclosure surface, during windy conditions which intensi- t = h (2u∗)−1 s (2.36) m m fied in the subsequent few days. A near-uniform Following this logic, a wind of 8 m s−1 may be distribution with depth was quickly established expected to mix a 20-m epilimnion in 2000 s (33 (see Fig. 2.20). The spores (d = 32.80 ± 3.18; −3 minutes) but a 2-m layer in just 200 s (3.3 min- ρc = 1049 kg m ; ϕr ∼ 2.2) had a measured sink- −1 −1 ◦ utes). A wind speed of 4 m s would take twice ing rate (ws)of15.75 µms at 17 C, which, as long in either case. adjusted for the density and viscosity of the water These approximations are among the most at the 4–5 ◦Cobtaining in the field, predicted an important recent derivations pertaining to the in-situ intrinsic sinking rate of 0.96 m d−1. The environment of phytoplankton. They have a pro- theoretical time for spores to eliminate the enclo- found relevance to the harvest of light energy sure (at the time, H ∼ 11.8 m) was thus calcu- and the adaptations of species to maximise the lated to be (t = )12.3 days. In fact, the elimi- opportunities provided by turbulent transport nation proceeded smoothly, always from a near- (see Chapter 3). uniformly distributed residual population at an average exponential rate of −0.10 m d−1, which 2.6.6 Particle settling from variable mixed value corresponds to a 95% removal in (te =)30 layers: an experiment days. The ratio te/t is lower than predicted in Sec- As part of an effort to improve the empirical tion 2.6.2 (2.44 against 3.0). This may be explained description of the sedimentary losses of phyto- by probable violation of the initial assumption of plankton from suspension, Reynolds employed full mixing of the water column throughout the several approaches to measuring the sedimentary experiment. Although no significant density gra- flux in the large limnetic enclosures in Blelham dient developed, continuous and complete verti- Tarn, UK. These cylindrical vessels, 45 m in diam- cal mixing of the enclosure cannot be verified. eter, anchored in 11–12 m of water contained Nevertheless, the outcome is sufficiently close to sufficient water (∼18 000 m3)tobehavelikenat- themodel (Fig. 2.20)solution for us not to reject ural water columns. Their hydraulic isolation thehypothesis that entrained particles are lost ensured all populations husbanded therein were from suspension at an exponential rate close to captive and virtually free from external contami- −(ws/hm). nation (Lack and Lund, 1974;LundandReynolds, In the second experiment, commenced in 1982;seealso Section 5.5.1). The deployment of June, spores were dispersed at the top of the THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 77

Figure 2.20 Modelled (M) and actual (A) depth–time distributions of preserved Lycopodium spores (of predetermined sinking characteristics) introduced at the water surface of one of the Blelham enclosures on each of three occasions (1, 9 January; 2, 3 June; 3, 9 September) during 1976, under sharply differing conditions of thermal stability. Lycopodium concentrations plotted as cylindrical curves; density gradients plotted as dashed lines. ∗ – indicates no ﬁeld data are available. Redrawn from Reynolds (1984a).

stratified enclosure during relatively calm con- mixed-layer deepening. Variability in wind forc- ditions. Sampling within 30 minutes showed a ing was quite high and a certain degree of re- good dispersion but still restricted to the top 1 entrainment is known to have occurred but the monly.However,4dayslater, spores were found time taken to achieve 95% elimination from at all depths but the bulk of the original addition theupper9mofthewatercolumn(te = 18.0 was accounted for in a ‘cloud’ of spores located days) at the calculated in-situ sinking rate (ws) at a depth of 5–7 m. After a further 7 days, mea- of 1.32 m d−1 exceeded the equivalent t value surable concentrations were detected only in the (9/1.32 = 6.82) by a factor of 2.6. bottom2mofthecolumn,meaningthat, effec- The three results are held to confirm that the tively, the addition had cleared 10 m in 11 days, depth of entrainment by mixing is the major con- at a rate not less than 0.91 m d−1.Adjusted for straint on elimination of non-motile plankters the density and viscosity of the water atthetop heavier than water, that the eventual elimina- of the water column, the predicted sinking rate tion is however delayed rather than avoided, and was 1.42md−1. Thus, overall, the value of t for that prolongation of the period of suspension is the first10m(= 7days)wasexceededbythe in proportion to the depth of the mixed layer, ∗ observed te (= 11 days) by a factor of only 1.57. Part wherein u ≥ 15 (ws). of the explanation is that sinking spores would have sunk more slowly than 1.42 m d−1 in the colder hypolimnion. However, the model expla- 2.7 The spatial distribution of nation envisages a daily export of the population from the upper mixed layer (varying between 0.5 phytoplankton and 4 m during the course of the experiment), calculated as N exp −(ws/hm), whence it contin- The focus of this chapter, the conditions of −1 ues to settle unentrained at the rate ws md .To entrainment and embedding of phytoplankton in judge fromFig.2.20,this is an oversimplification the constant movement of natural water masses, but the prediction of the elimination is reason- is now extended to the conditions where water able. movements are either insufficiently strong or The same model was applied to predict the insufficiently extensive to randomise the spa- distribution and settlement of Lycopodium spores tial distribution of phytoplankton. This section in the third experiment, conducted during the is concerned with the circumstances of plankters autumnal period of weakening stratification and becoming disentrained and the consequences of 78 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

weakening entrainment for individuals, popula- can respond (for instance, light fluctuations are tions and communities, as augured by spatial dif- more frequent than cell division) or so much less ferentiation in the vertical and horizontal distri- rapidly that it is perceived as a constant (such as butions of natural assemblages. annual temperature fluctuations having a much Distributional variation is subject to issues of lower frequency than cell division) which will scaling which need to be clarified. It has already be no more relevant to today’s populations than been made plain that aquatic environments are is the onset of the next ice age to the mainte- manifestly heterogenous, owing to spatial differ- nance of present-day forests (Reynolds, 1993b). In ences in temperature, solute content, wind stress, between, where driver and response scales are etc., and that each of these drivers is itself sub- more closely matched, the interactions are rather ject to almost continuous variation. However, more profound, as in the frequency with which while precise values are impossible to predict, new generations are recruited to a water col- the range of variability may be forecast with umn mixed to a different extent on successive some confidence, either on the basis of averag- days. ing or experience, or both. We may not be able The variability in the instantaneous distribu- to predict the intensity of wind mixing in a tion of phytoplankton may be considered in rela- lake some three weeks or more into the future tion to an analogous spatial scale. Consider first a but we may estimate from the knowledge base randomised suspension of unicellular flagellates, the probability with which a given wind inten- such as Chlamydomonas or Dunaliella.Viewedat sity will prevail. The changes in temperature, the 1–10 µmscale, distribution appears highly insolation, hydraulic exchanges and the delivery patchy, resolvable on the basis of presence or of essential nutrients affecting a given stretch absence. In the range 10–1000 µm, the same dis- of water also occur on simultaneously differ- tribution is increasingly perceived to be near- ing scales of temporal oscillation – over minutes uniform but, in the turbulence field of a wind- to hours, night–day alternations, with changing mixed layer, variability over the 1–10 mm scale season, interannually and over much broader may attest to the interaction of algal movements scales of climatic change. The nesting of the with water at the viscous scale (Reynolds et al., smaller temporal scales within the larger scales 1993a). In the range 10–100 mm and, perhaps, holds consequences for phytoplankters in the 10–1000 mm, the distribution may again appear other direction, too, towards the probabilities of uniform. Beyond that, the increasing tendency being ingested by filter-feeders, of the adequacy forthere to be variations in the intensity of mix- of light at the depths to which entrained cells ing leads to the separation of water masses in may be circulated, even to the probability that thevertical (at the scale of tens to hundreds the energyofthenext photon hitting the photo- of metres) and in the horizontal (hundreds of synthetic apparatus will be captured. The point metres to hundreds of kilometres), at least to is that the reactions of individual organelles, theextent that they represent quite isolated and cells, populations and assemblages are now gen- coexisting environments, each having quite dis- erally predictable, but the impacts can only be tinct conditions for the survival of the flagel- judged at the relevant temporal scales. These lates and the rate of their recruitment by growth. responses and their outcomes are considered in This is but one example of the principle that the later chapters in the context of the relevant pro- relative uniformity or heterogeneity within an cesses (photosynthesis, assimilation, growth and ecological system depends mainly upon the spa- population dynamics). However, the interrelation tial and temporal scale at which it is observed of scales makes for fascinating study (see, for (Juhasz-Nagy,´ 1992). instance, Reynolds, 1999a, 2002a): in the end, Uniformity and randomisation, on the one thedistinction is determined by the reactivity of hand, and differentiation (‘patchiness’), on the the response. This means that critical variations other, may thus be detected simultaneously alter more rapidly than the process of interest within a single, often quite small system. THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 79

Moreover, the biological differentiation of indi- agradient between the layers persists, albeit by vidual patches may well increase the longer their now at a greater physical depth). Internal waves mutual isolation persists. Thus it remains impor- may form as a consequence of differential veloci- tant to make clear the spatial scale that is under ties, mirroring those formed at the water surface consideration, whether in the context of vertical by the drag ofhigh-velocity winds; and, just as or horizontal distribution. surface waves break when the velocity differences can no longer be contained, so internal waves 2.7.1 Vertical distribution of phytoplankton become unstable and collapse (Kelvin–Helmholtz Against this background, it seems appropriate instabilities:see, e.g., Imberger, 1985,fordetails), to emphasise that the expectation of the verti- releasing more bottom water into the upper con- cal distributions of phytoplankton is that they vection. should conform to the vertical differentiation of In shallow water columns, the extension of thewater column, in terms of its current (or, the convective layer is confined to the physi- at least, very recent) kinetic structure. The lat- cal water depth, in which all energy-dissipative ter may comprise a wind-mixed convective layer interactions and return flows must be accommo- overlying a typically less energetic layer of turbu- dated. This necessarily results in very complex lence that is supposed to diminish with increas- and aggressive mixing processes, often extending ing depth, towards a benthic boundary layer in to thebottom boundary layer and, on occasions, which turbulence is overcome by friction with penetrating it to the extent of entraining, and the solid surface. However, in the seas as in resuspending, the unconsolidated sedimented lakes, the horizontal drift of the convective layer material. has to be compensated by counterflows, which Supposing wind-driven convective layers movement promotes internal eddies and provides everywhere to be characterised by u∗ ≥ 5 × some turbulent kinetic energy from below. The 10−3 ms−1 (i.e. 5 mm s−1), they should be capa- formation of vertical density gradients may allow ble of fulfilling the entrainment criterion for the confinement of the horizontal circulation to plankton with sinking, floating or swimming the upper part of the water column, leaving a dis- speeds of ≤250 × 10−6 ms−1.Comparison with tinct and kinetically rather inert water mass of Section 2.6.1 supports the deduction that the the pycnocline, with very weak vertical motion. distribution of almost all phytoplankters must Density gradients form at depths in large, deep be quickly randomised through the vertical lakes and in the sea but do not contain basin- extent of convective layers. However, if the wide circulations; even though the gradients may driving energy weakens, so that the convective persist, they may be rhythmically or chaotically layer contracts (in line with the Monin–Obukhov displaced through the interplay of the gravita- prediction [Eq. 2.31]or, without simultaneous tional ‘sloshing’ movements of deep water masses heat gain, because u∗ diminishes), plankters that and the convective movements of the surface were entrained towards the bottom of the layer layer. become increasingly liable to disentrainment in The vertical extent of the convective layer is, situ, where, ergo,their own intrinsic movements as we have seen, highly variable and subject to begin to be expressed. change at high frequency. It can vary from a few Four examples of distributional responses to millimetres to tens of metres over a period of physical structure are sufficient to demonstrate hours and between tens to hundreds of metres thebasic behaviours of phytoplankters that are over a few days. The presence of density gradients heavier than water (ρc >ρw), those that are fre- reduces the entrainability of the deeper water quently lighter than water (ρc <ρw), those non- into the surface flow. There is often great com- motile species that are more nearly isopycnic plexity at the interface (note, even if the top layer (ρc ∼ ρw)and those that are sufficiently motile for of the deeper water is sheared off and incorpo- any density difference to be at times surmount- rated intotheconvective circulation of the upper, able. The selection also employs some of the 80 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

While numerous other factors intervene in the seasonal population dynamics and periodicity of diatoms, the importance of the depth of the surface mixed layer as another ecological threshold that must be satisfied for successful maintenance and recruitment of diatoms has been demonstrated many times (Reynolds and Wise- man, 1982;Reynolds et al., 1983b; Sommer, 1988a; Huisman et al., 1999;Padisak´ et al., 2003b). If therate of recruitment through cell growth and replication fails to make good the aggregate rate of all losses, including to settlement, then the standing population must go into decline. The extent of the mixed depth is already implicated in the ability of a seed population to remain Figure 2.21 Depth–time plot of the vertical distribution of in suspension. As the Lycopodium experiments Asterionella formosa in the North Basin of Windermere demonstrate (see Section 2.6.6), the nearer this through 1947. Isopleths in live cells mL−1. The shaded area contracts to the surface, the faster is the rate of represents the extent of the metalimnion. Original from Lund loss from the diminishing mixed layer itself and et al.(1963), and redrawn from Reynolds (1984a). from the enlarging, stagnating layer beneath it. This occurs independently of the chemical capacity of the water to support growth, although it is differing ways that distributional data may be often influenced by spontaneous changes in the represented. intrinsic sinking rate (Reynolds and Wiseman, 1982;Neale et al., 1991b). Non-motile, negatively buoyant plankters The plot of Lund et al.(1963)(Fig. 2.21)shows (ρc >ρw) thestrong tendency in the first 3 months of the Forthe first case, the classical study of Lund year towards vertical similarity in the concentra- et al.(1963)ontheseason-long distribution of tion of Asterionella (with the isopleths, in cells Asterionella cells in the North Basin of Winder- mL−1,themselves vertically arranged), as their mere in 1947 is illustrated (Fig. 2.21). The den- numbers slowly rise during the spring increase. sities of diatoms mostly exceed, sometimes con- With the progressive increase in day length and siderably, that of the surrounding water in lakes potential intensity of solar irradiance, the lake and seas. Those bound to be negatively buoy- starts to stratify, with a pycnocline (represented ant (they have positive sinking rates) are des- in Fig. 2.21 by the fine stippling) developing at a tined to be lost progressively from suspension, depth of between 5 and 10 m from the surface. at variable rates that are due to the relation- The contours reflect the segregating response of ship between the (variable) intrinsic particle sink- thevertical distribution, with an initial near- ing rate and the (variable) depth of penetration surface acceleration in recruitment but followed of sufficient kinetic energy to fulfil the species- soon afterwards by rapid decline in numbers, specific entrainment criterion. Even before the as sinking losses by dilution from the truncated critical quantities were known, numerous stud- mixed layer overtake recruitment. The distribu- ies had demonstrated the sensitivity of diatom tion of contours beneath the pycnocline acquire a distribution to water movements and to the diagonal trend (reflecting algal settlement) while onset of thermal stratification in particular, both thenear-horizontal lines in the pycnocline itself in lakes (Ruttner, 1938;Findenegg, 1943;Lund, confirm the heterogeneity of numbers in the ver- 1959;Nauwerck, 1963)and in the sea (Mar- tical direction and the strong vertical gradient galef, 1958, 1978;Parsons and Takahashi, 1973; in algal concentration in the region of the pyc- Smayda, 1973, 1980;Holliganand Harbour, 1977). nocline. It is not until the final breakdown of THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 81 thermal stratification (usually in December in Windermere) that approximate homogeneity in thevertical is recovered.

Positively buoyant plankters (ρc <ρw) The vertical distribution of buoyant organisms, which include many of the planktic, gas- vacuolate Cyanobacteria during at least stages of their development, is similarly responsive to variability in the diffusive strength of vertical convection, save that algae float, rather than sink, through the more stable layers. A further difference is that the population of the upper mixed layer potentially experiences concentration by net recruitment from upward-moving organisms rather than dilution as downward-moving organ- Figure 2.22 Changes in the vertical distribution of isms are shed from it. Microcystis aeruginosa colonies in a small lake (shown as It has long been appreciated that the forma- cylindrical curves) in relation to temperature (isopleths ◦ / tion of surface scums of buoyant Cyanobacteria in C), during 28 29 July, 1971 (SS, sunset; SR, sunrise). Data of Reynolds (1973b) and redrawn from Reynolds (1984a). (variously known, colloquially and in many lan- guages, as water blooms, flowering of the waters, etc.: Reynolds and Walsby, 1975), and involving anticyclonic weather in July 1971. The colonies such genera as Anabaena, Anabaenopsis, Aphani- were, on average, buoyant throughout, having zomenon, Gloeotrichia, Gomphosphaeria, Woronichinia amean flotation rate of ∼9 µms−1 during the and (especially) Microcystis are prone to form in first day that increased almost twofold during still, windless conditions (Griffiths, 1939). Buoy- the hours of darkness (Reynolds, 1973b). Note ant Trichodesmium filaments also form locally that an established temperature gradient, extend- dense surface patches in warm tropical seas ing downwards from a depth of about 3.5 m, under calm conditions (Ramamurthy, 1970): the already contained the buoyant population and little flakes of filaments also merited the sailors’ the changing vertical distribution of Microcystis colloquialism of ‘sea sawdust’. occurred in relation to the secondary microstratifi- The mechanisms of scum formation are not cation that developed during the course of the day straightforward but, rather, require the coinci- (density gradient 0.1 kg m−3 m−1). A light breeze dence of three preconditions: a pre-existing pop- occurred in the early evening of 28 July, before ulation, a significant proportion of this being windless conditions resumed. Some convectional rendered positively buoyant on the balance of cooling also occurred during the night, suffi- its gas-vesicle content, and the hydrographic con- cient to redistribute the population to a small ditions being such as to allow their disentrain- extent but not to dissipate the surface scum that ment (Reynolds and Walsby, 1975). The present had formed, which, from an average concentra- discussion assumes that the first two criteria are tion of ∼160 colonies mL−1,increased 37-fold (to satisfied, scum formation now depending upon 5940 mL−1 at 23.30). the relatively short-term onset of lowered diffu- The method of plotting, greatly favoured by sivity to the water surface, so that the magni- theearly plankton ecologists, invokes the use of tude of the flotation velocity (−ws)isnolonger ‘cylindrical curves’. These are drawn as laterally overwhelmed by the turbulent velocity (u∗). The viewed solid cones or more complex ‘table-legs’, example presented in Fig. 2.22 traces the chang- thecross-sectional diameter at any given point ing distribution of colonies of Microcystis aerug- being proportional to the cube root of the con- inosa,inrelation to the thermal structure in a centration. These shapes capture well the discon- small temperate lake during one 24-h period of tinuities in a given vertical distribution but may 82 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

(where, regardless of density, small size determines a low Stokesian velocity) and among rather larger, mucilage-invested phytoplankters, which are genuinely able to ‘dilute’ the excess mass of cell protoplasm and structures in the relatively large volume of water that the mucilaginous sheath immobilises. In either case, the adaptations to pelagic survival take the organisms closest to the ideal condition for suspension. These are, literally, the most readily entrainable plankters according to the definition (Section 2.6.1, Figure 2.23 The relationship between vertical patchiness Eq. 2.19). of Microcystis in the shallow Eglwys Nynydd reservoir and In Fig. 2.24,sequences in the vertical dis- wind velocity (U). Data of George and Edwards (1976) and tributions of two non-motile green algae – redrawn from Reynolds (1984a). thenanoplanktic chlorococcal Ankyra and the microplanktic, coenobial palmelloid Coenochloris be less helpful than contoured depth–time plots (formerly ascribed to Sphaerocystis)–aredepicted (such as usedinFig.2.21)overlongperiods of in relation to stratification in the large limnetic time. Neither do they necessarily convey the gen- enclosures in Blelham Tarn. The original data eralism between vertical discontinuity and the refer to average concentrations in metre-thick lay- physical heterogeneity. In consideration of a 2- ers (sampled by means of a 1-m long Friedinger year series of Microcystis depth profiles in a small, trap: Irish, 1980)orinmultiples thereof. The shallow reservoir, (Eglwys Nynydd: area 1.01 km2, data are plotted as stacks of individual cylin- mean depth 3.5 m), George and Edwards (1976) ders, the diameters of which correspond to the ∗ calculated a crowding statistic (x ,owingtoLloyd, respective cube roots of the concentrations. In 1967)anditsratiotothemean concentration both cases, the algae are dispersed approximately over the full depth (¯x)todemonstrate the sus- uniformly through the epilimnion, while num- ceptibility of vertical distribution to the wind- bers in the hypolimnion remain low, owing to ∗ forced energy. Putting x = [¯x + s2/x¯ − 1], where weak recruitment either by growth or by sedi- 2 −1 s is the variance between the individual sam- mentation (ws < 0.1md ). The effect of grazers ples in each vertical series, they showed that the has not been excluded but simultaneous stud- ∗ relative crowding in the vertical, (x /x¯), occurred ies on loss rates suggest that the impact may − only at low wind speeds (U < 4ms 1)andin have been small, while neither species was well- approximate proportion to U), but wind speeds represented in simultaneous sediment-trap col- − over 4ms 1 were always sufficient to randomise lections or samples from the surface deposits Microcystis through the full 3.5-m depth of the (Reynolds et al., 1982a). On the other hand, deep- reservoir (Fig. 2.23). ening of the mixed layer and depression of thethermocline result in the immediate ran- Neutrally buoyant plankters (ρc ∼ ρw) domisation of approximately neutrally buoyant In this instance, ‘neutral’ implies ‘approximately algae throughout the newly expanded layer. Such neutral’. As already discussed above (Section 2.5), species are thus regarded as being always likely it is not possible, nor particularly desirable, for to become freely distributed within water lay- plankters to be continuously isopycnic with the ers subject to turbulent mixing, then to settle medium. Nevertheless, many species of phyto- from them only very slowly and, of course, to plankton that are non-motile and are unencum- be unable to recover a former distribution when bered by skeletal ballast (or the gas-filled spaces mixing weakens (Happey-Wood, 1988). to offset it) survive through maintaining a state ∗ in which they do not travel far after disentrain- Motile plankters (us > u ) ment. This state is achieved among very small Flagellates and ciliates are capable of directed unicells of the nanoplankton and picoplankton movements that, actually as well as potentially, THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 83

Figure 2.24 Instances in the vertical distribution of non-motile phytoplankton in a Lund Enclosure during the summer of 1978, shown as cylindrical curves. Ankyra is a unicellular nanoplankter; Coenochloris occurs as palmelloid colonies. Redrawn from Reynolds (1984a).

may result in discontinuous vertical distributions vertical heterogeneity of flagellate distribution in lakes and seas. This ability is compounded by in ponds, lakes and coastal embayments. Ref- the capacity for self-propulsion of the alga (the erence to no more than a few investigative word ‘swim’ is studiously avoided – see Section studies is needed (Nauwerck, 1963; Moss, 1967; 2.3.4). In terms of body-lengths per unit time, Reynolds, 1976a;Cloern, 1977; Moll and Stoer- the rates of progression may impress the micro- mer, 1982; Donato-Rondon, 2001). Works detail- scopist but, in reality, rarely exceed the order of ing behaviour of particular phylogenetic groups 0.1–1 mm s−1. include Ichimura et al.(1968) and Klaveness (1988) In general, the rates of progress that are pos- on cryptomonads; Pick et al.(1984) and Sandgren sible in natural water columns are related to (1988b)onchrysophytes; Croome and Tyler (1984) size and to the attendant ability to disentrain and Hader¨ (1986)oneuglenoids. Note also that from the scale of water movements (Sommer, not all flagellate movements are directed towards 1988b). Moreover, the detectable impacts on ver- the surface. There are many instances of con- tical distribution also depend upon some direc- spicuous surface avoidance (Heaney and Furnass, tionality in the movements or some common set 1980; Heaney and Talling, 1980a;Galvez´ et al., of responses being simultaneously expressed: if 1988;Kamykowski et al., 1992)andofassembling all movements are random, fast rates of move- deep-water ‘depth maxima’ of flagellates, analo- ment scarcely lead to any predictable pattern of gous to those of Planktothrix and photosynthetic distribution. For instance, the impressive verti- bacteria (Vicente and Miracle, 1988;Gasol et al., cal migrations of populations of large dinoflag- 1992). ellates are powerfully and self-evidently respon- The example illustrated in Fig. 2.25 shows the sive to the movements of individual cells within contrasted distribution of Ceratium hirundinella. environmental gradients of light and nutrient This freshwater dinoflagellate is known for its availability. This applies even more impressively strong motility (up to 0.3 mm s−1)(see Section to the colonial volvocalean migrations (Section 2.6.1) and its well-studied capacity for vertical 2.6.1) where all the flagellar beating of all the migration under suitable hydrographic condi- cells in the colony have to be under simultaneous tions (Talling, 1971;Reynolds, 1976b; Harris et al., control. The point needs emphasis as the flagellar 1979; Heaney and Talling, 1980a, b;Frempong, movements of, for instance, the colonial chrys- 1984;Pollingher, 1988; James et al., 1992). These ophytes (including the large and superficially properties enable it quickly to take up advan- Volvox-like Uroglena), seem less well coordinated: tageous distribution with respect to light gradi- they neither ‘swim’ so fast, nor do their move- ents, when diffusivity permits (u∗ < 10−4 ms−1). ments produce such readily interpretable distri- The right-hand profile in Fig. 2.25 shows the butions as Volvox (Sandgren, 1988b). vertical distribution of Ceratium during windy On the other hand, there is a large num- weather in a small, eutrophic temperate lake; ber of published field studies attesting to the theleft-hand profile shows a distribution under 84 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Figure 2.25 Contrasted vertical distributions of the motile dinoﬂagellate Ceratium hirundinella,in a small stratifying lake (Crose Mere, UK), in relation to temperature gradients (θ) and percentage light penetration (pecked lines). (a) was observed under very calm conditions; (b) under strong winds. Redrawn from Reynolds (1984a).

only weakly stratified conditions but one that is ing significant or systematic differences in con- strongly allied to the light gradient. centration. There have been few systematic attempts to 2.7.2 Horizontal distribution of resolve this question directly. In a rarely cited phytoplankton study, Nasev et al.(1978)analysed the confidence A considerable literature on the horizontal vari- interval about phytoplankton counting by parti- ability in plankton distribution has grown up, tioning the variance attaching to each step in the seemingly aimed, in part, towards invalidating estimation – from sampling through to count- any preconceived assumption of homogeneity. It ing. Provided adequate steps were taken to sup- is difficult to determine just where this assump- press the errors of subsampling and counting tion might have arisen, as investigations readily (Javorniˇcky, 1958;Lundet al., 1958;Willén, 1976), demonstrate that distributions are often far from systematic differences in the numbers present in homogeneous. It may be that a predominance theoriginal samples could be detected at scales of of papers in the mid-twentieth century focused afew tens of metres but, on other occasions, not on the population dynamics and vertical distri- for hundreds. Irish and Clarke (1984)analysed the butions of phytoplankton in small lakes paying estimates of specific algal populations of algae in insufficient attention to simultaneous horizon- similar samples collected from within the con- tal heterogeneity. Such assumptions, real or sup- fines of a single Blelham enclosure (area 1641 m2, posed, have no place in modern plankton science. diameter, 45.7 m) at locations nominated on a However, even now, it is important to present a stratified-random grid. They found that the coeffi- perspective on just how much variation might be cients of variation varied among different species expected, over what sort of horizontal distances of plankton, from about 5%, in the case of non- and how it might reflect the contributory physi- motile, neutrally buoyant algae, to up to 22% cal processes. forsome larger, buoyancy-regulating Cyanobacte- ria. In another, unrelated study, Stephenson et al. Small-scale patchiness (1984), showed that spatial variability increased Omitting the very smallest scales (see pream- with increasing enclosure size. ble to Section 2.7), phytoplankton is generally Ageneral conclusion is that sampling designs well-randomised within freshly collected water underpinning in-situ studies of phytoplankton samples (typical volumes in the range 0.5–5 population dynamics must not fail to take notice litres, roughly corresponding to a linear scale of of the horizontal dimension. However, the size 50–200 mm). Thus, there is normally a low coeffi- of the basin under investigation is also impor- cient of variation between the concentrations of tant. For instance, a coefficient of variation of plankton in successive samples taken at the same even 22% is small compared with the outcome place. The first focus of this section is the hori- of growth and cell division, where a popula- zontal distance separating similar samples show- tion doubling represents a variation of 100% per THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 85

Box 2.1 Langmuir circulations

Langmuir circulations are elongated, wind-induced convection cells that form at the surface of lakes and of the sea, having characters first formalised by Langmuir (1938). They take the form of parallel rotations, that spiral approximately in the direction of the wind, in the general manner sketched in Fig. 2.26. Their structure is more clearly understood than is their mechanics but it is plain that the cells arise through the interaction of the horizontal drag currents and the gravitational resistance of deeper water to entrainment. Thus, they provide the additional means of spatially confined energy dissipation at the upper end of the eddy spectrum (Leibovich, 1983). In this way, they represent a fairly aggressive mixing process at the mesoscale but the ordered structure of the convection cells does lead naturally to a surprising level of microstructural differentiation. Adjacent spirals have interfaces where both are either upwelling simultaneously or downwelling simultaneously. In the former case, there is a divergence at the surface; in the latter there is a convergence. This gives rise to the striking formation of surface windrows or streaks that comprise bubbles and such buoyant particles as seaweed fragments, leaves and plant remains, insect exuviae and animal products as they are disentrained at the convergences of downwelling water. The dynamics and dimensions of Langmuir circulation cells are now fairly well known. The circumstances of their formation never arise at all at low wind speeds (U < 3–4 m s−1: Scott et al., 1969; Assaf et al., 1971). Spacing of streaks may be as little as 3–6 m apart at these lower wind speeds, when there is an rough correlation between the downwelling depth and the width of the cell (ratio 2.0–2.8). In the open water of large lakes and the sea, where there is little impediment to Langmuir circulation, the distance between the larger streaks (50–100 m) maintains this approximate dimensional proportionality, being comparable with that of the mixed depth (Harris and Lott, 1973;Boyce, 1974). The velocity of downwelling (w > 2.5 × 10−2 ms−1)issaid to be proportional to the wind speed (∼0.8 × 10−2 U): Scott et al., 1969; Faller, 1971), but the average velocities of the upwellings and cross-currents are typically less. Consequences for microalgae have been considered (notably by Smayda, 1970, and George and Edwards, 1973) and are reviewed in the main text. generation time (Reynolds, 1986b). Moreover, a The mechanism concerns the Langmuir circula- spatial difference within a closed area of water tions, which are consequent upon a strong wind only 45.7 m across is unlikely to persist, as the acting on a shallow surface layer, when acceler- forcing of the gradient is hardly likely to be ated dissipation from a spatially constrained vol- stable. A change in wind intensity and direc- ume generates ordered structures. These are man- tion is likely to redistribute the same population ifest as stripe-like ‘windrows’ of foam bubbles within the same limited space. on the water surface. Even now, the formation We may follow this progression of thinking of Langmuir cells is imperfectly understood but to the wider confines of an entire small lake, their main properties are fairly well described or to the relatively unconfined areas of the open (see Box 2.1). sea. Before that, however, it is opportune to draw Although the characteristic current veloc- attention to a relatively better-known horizon- ities prevalent within Langmuir circulations tal sorting of phytoplankton at the scale of a (>10–20 mm s−1)would be well sufficient to few metresand,curiously perhaps, is dependent entrain phytoplankton around the spiral trajec- upon significant wind forcing on the lake surface. tories, the cells do have identifiable relative dead 86 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Figure 2.26 Diagrammatic section across wind-induced surface ﬂow to show Langmuir circulations. Redrawn from Reynolds (1984a).

Figure 2.27 Schematic section through Langmuir rotations to show the likely distributions of non-buoyant (•), positively buoyant () and neutrally buoyant, fully entrained (∗) organisms. Based on an original in George (1981) and redrawn from Reynolds (1984a).

spots, towards the centre of the spiral, at the persistence (Evans and Taylor, 1980). Whereas it base of the upwelling and, especially, at the top may take some minutes to organise and generate of the convergent downwellings, marked by the thecirculation, a wind of fluctuating speed and foamlines (see Fig. 2.26). Smayda (1970)predicted direction will be constantly initiating new pat- the distributions of planktic algae, categorised by ternsand superimposing them on previous ones. their intrinsic settling velocities, within a cross- This behaviour does not suppress the fact that section adjacent to Langmuir spirals. Indepen- larger, more motile plankters remain liable to dent observations by George and Edwards (1973) crude sorting, on the basis of their individual and Harris and Lott (1973)onthedistributions buoyant properties, into a horizontal patchiness of real (Daphnia)andartificial (paper) markers in at the relatively small scales of a few metres to a thefield lent support for Smayda’s predictions. few tensofmetres. Although mostly well-entrained, sinking particles (ρc >ρw)takelongertocleartheupwellingsand Patchiness in small lake basins accumulate selectively there, buoyant particles With or without superimposed Langmuir spirals, (ρc <ρw)willsimilarlytakelonger to clear the the horizontal drift is likely, at least in lakes, to downwellings and those entering the foamline be interrupted by shallows, margins or islands, will tend to be retained. A schematic, based on where the flow is subject to new constraints. Sup- figures in Smayda (1970)andGeorge (1981), is posing that little of the drifting water escapes included as Fig. 2.27. thebasin, most is returned upwind in subsur- Such distributions of algae are not easy to ver- face countercurrents (see Imberger and Spigel, ify by traditional sampling–counting methods, 1987). In small basins, there is a clear horizon- because the behaviour depends not only on the tal circulation, which George and Edwards (1976) match of the necessary physical conditions – the analogised to a conveyor belt. While this process circulating velocity, the width and penetration of seems destined towards the basin-scale horizon- the rotations are all wind-influenced – but their tal integration of populations, the movements of THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 87

Figure 2.28 Whole-lake ‘conveyor belt’ model of non-buoyant (•) and positively buoyant (◦)phytoplankters, proposed by George and Edwards (1976). Redrawn from Reynolds (1984a).

plankters in the vertical plane may well super- impose a distinct advective patchiness in the horizontal plane. The mechanism is analogous to the behavioural segregation in the Langmuir circulation, though on a larger scale. Put simply, the upwardmovement of buoyant organisms is enhanced in upwind upwellings but resisted in downwind downwellings; conversely, sinking organisms accelerate in downwellings but accumulate in the upcurrents. Positively buoyant organisms accumulate on downwind (lee) shores; negatively buoyant organisms are relatively more Figure 2.29 Advective horizontal patchiness of abundant to windward (Fig. 2.28). phytoplankters in relation to wind direction: (a) positively Such distributions of zooplankton have been buoyant Microcystis in Eglwys Nynydd reservoir (after George observed, with concentrations of downward- and Edwards, 1976), isopleths in µg chlorophyll a L−1; (b) swimming crustaceans collecting upwind (Cole- surface-avoiding, motile Ceratium in Esthwaite Water (after −1 brook, 1960;GeorgeandEdwards, 1976). Simi- Heaney, 1976), isopleths in cells mL . Redrawn from lar patterns have been described for downward- Reynolds (1984a). migrating dinoflagellates (Heaney, 1976;George and Heaney, 1978); on the other hand, the downwind accumulation of buoyant Microcystis has been verified graphically by George and Edwards (1976). Representative maps of these contrasting outcomes are shown in Fig. 2.29. The representation in Fig. 2.29aisoneof a number of such ‘snapshots’ of variable patchiness during a long period of Microcystis dominance in the Eglwys Nynydd reservoir. The field data allowed George and Edwards (1976)tocalculate a crowding index of horizontal patchiness (x∗), analogous to that solved for the vertical dimension (See Section 2.7.1), and to show that its relationship to the mean population (¯x) wasaclose correlative of the accumulated wind Figure 2.30 The relationship between horizontal effect. Their data are redrawn here (Fig. 2.30)but patchiness of Microcystis in the shallow Eglwys Nynydd with the horizontal axis rescaled as an equiva- reservoir and wind velocity (U). Data of George and Edwards lent steady wind speed. Patchiness is strongest (1976) and redrawn from Reynolds (1984a). 88 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

Large-scale patchiness Nevertheless, the relationship does have a time dimension, the horizontal mixing time, and this may accommodate other sources of change. For instance, if a constant wind of 4 m s−1 induces asurface drift of the order of 400 m d−1 across a1-km basin, the probable mixing time is 5 d. If, in the same 5 d, a patchy population is recruited through one or more successive doublings, then the same probability of its achieving uniformity requires stronger forcing or a shorter mixing time. This relationship between transport and recruitment becomes increasingly prevalent in larger lake basins where the role of the return current in establishing uniformity is progressively diminished: maintenance of large- scale patches (kilometers, days) needs persistent spatial differences in recruitment rate. The latter might be due directly to a local enhancement Figure 2.31 Relationships between horizontal and vertical in organismic replication (because of warm or patchiness of Microcystis (•, Figures 2.23, 2.30) and of Daphnia shallow water, or a point source of nutrient) or populations (◦)inEglwys Nynydd reservoir, as detected by to consistently enhanced removal rates by local George and Edwards (1976). Redrawn from Reynolds aggregations of herbivorous animals. However, (1984a). to be evident at all, the patch must give way to the concentrations in a surrounding larger stretch ofwater,through diffusion and erosion by hydraulic exchanges at the periphery. Sev- when winds are light but it weakens as winds eral publications have considered this relation- start toexceed3ms−1,disappearing altogether ship. Two of these, in particular (Skellam, 1951; at U > 5ms−1. The work on Ceratium in Esthwaite Kierstead and Slobodkin, 1953), have given us the Water (Heaney, 1976;GeorgeandHeaney, 1978; so-called KISS explicative model, relating the criti- Heaney and Talling, 1980a, b)pointsconsistently cal size of the patch to the interplay between the to the development of horizontal patchiness only ratesofreproductive recruitment and of horizon- at wind speeds < ∼4ms−1. tal diffusivity. Specifically, Kierstead and Slobod- Apart from illustrating the link between ver- kin (1953)predicted the radius of a critical patch tical behaviour of phytoplankton and its horizon- (rc)as: tal distribution in small lakes, confirmed in the r = 2.4048(D /k )2 (2.37) statistical interaction of horizontal and vertical c x n patchiness shown in Fig. 2.31,theinformation where Dx is the horizontal diffusivity and kn is considered in this section helps to establish a thenet rate of population increase or decrease. general point about the confinement of water Interpolating values for kn appropriate to the gen- motion to a basin of defined dimensions. It is that eration times of phytoplankton (the order of 0.1 once a critical level of forcing is applied, a certain to 1.0 doublings per day) and for typical wind- −3 −6 degree of uniformity is reimposed. It is not that driven diffusivities (Dx ∼ 5 × 10 to 2 × 10 the small-scale patchiness disappears – all the cm2 s−1:Okubo, 1971), critical radii of 60 m to causes of its creation remain intact – so much as 32 km may be derived. This 3-order range spans that the variance at the small scales becomes very thegeneral cases of large-scale phytoplankton similar at larger ones: small-scale heterogeneity patches in the open ocean considered by (for collapses into large-scale homogeneity. instance) Steele (1976), and Okubo (1978), with THE SPATIAL DISTRIBUTION OF PHYTOPLANKTON 89 themost probable cases having a critical min- large, northern continental lakes is the vernal imum of ∼1km(reviewofPlatt and Denman, patchiness of phytoplankton attributable to the 1980;see also Therriault and Platt, 1981). early-season growth in the inshore waters that Even under the most favourable conditions are retained by horizontal temperature gradi- of low diffusivities and localised rapid growth, ents associated with the centripetal seasonal patches smaller than 1 km are liable to rapid dis- warming – the so-called ‘thermal bar’. This phe- persion. Moreover, wind-driven diffusivity may be nomenon, first described in detail by Munawar considerably enhanced by other horizontal trans- and Munawar (1975)inthe context of diatom port mechanisms, including by flow in river chan- growth in Lake Ontario, has been reported from nels (see Smith, 1975), tidal mixing in estuaries other large lakes: Issyk-kul (Shaboonin, 1982), (data of Lucas et al., 1999)and, in stratified small- Ladozhskoye, Onezhskoye (Petrova, 1986)and to-medium lakes, by internal waves (Stocker and Baykal (Shimarev et al., 1993,Likhoshway et al., Imberger, 2003;Wuest¨ and Lorke, 2003). In spite 1996). of this, some instances of small patch persistence In general, it is fair to say that the KISS model are on record. Reynolds et al.(1993a)reported is illustrative rather than deterministic, and it is aset of observations on an intensely localised only imprecisely applicable to a majority of small explosive growth of Dinobryon in Lake Balaton, fol- lakes subject to internal circulation and advec- lowing a mass germination of spores disturbed by tion. Here, the predictive utility of the later gen- dredging operations. The increase in cell concen- eral model derived by Joseph and Sendner (1958) tration within the widening patch was overtaken is sometimes preferred. The fitted equation is after a week or two, partly through dispersal in used to predict critical patch radius as a function thecirculation of the eastern basin of the lake of the advective velocity, us: and into that of the western end but, ultimately, r = 3.67(u /k ) (2.38) because the rates of Dinobryon growth and recruit- c s n −3 ment soon ran down. If kn is one division per day and us = 5 × 10 At the other end ofthescale, satellite-sensed ms−1 (roughly what is generated by a wind force −1 distributions of phytoplankton in the ocean of 4 m s ), rc ∼ 1.6 km. At five times therateof −3 −1 reveal consistent areas of relatively high biomass, horizontal advection (us = 25 × 10 ms ), the covering tens to hundreds of kilometres in some critical radius is increased to ∼8km.Again, the cases – usually shallow shelf waters, well supplied actual values probably have less relevance than by riverine outflows, or along oceanic fronts and does the principle that patchiness in phytoplank- at deep-water upwellings (see review of Falkowski ton developing in lake basins less than 10 km in et al., 1998). The size and long-term stability of diameter is likely to be temporally transient and these structures are due to the geographical per- not systematically persistent. sistence of the favourable conditions that maintain production (shallow water, enriched nutri- Relevance of patchiness ent supply) relative to the rates of horizontal Many of the mysteries of patchiness that con- diffusivity in these unconfined locations. cerned plankton scientists in the third quarter Such behaviour is observable in larger lakes, of the twentieth century may have been cleared especially where there are persistent gradients up, but the issue remains an important one, (chiefly in the supply of nutrients) that survive fortwo main reasons. One, self-evidently, lies in seiching. Enduring patchiness was memorably the designofsamplingstrategies. If the purpose demonstrated by Watson and Kalff (1981)along is merely to characterise the community struc- apersistent nutrient gradient in the ribbon- ture, much information may be yielded from like glacial Lake Memphrémagog (Canada/USA). infrequent samples collected at a single location Persistent gradients of phytoplankton concen- (Kadiri and Reynolds, 1993)but, as soon as the tration are evident from long-term surveys of exercise concerns the quantification of plankton theNorth American Great Lakes (Munawar and populations and the dynamics of their change, it Munawar, 1996, 2000). Of additional interest in is essential to intensify the sampling in both time 90 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

and space. Sampling design is covered in many theseasonal formation of cyanobacterial plates methodological manuals (see, for instance, Sour- in deep alpine lakes (Bright and Walsby, 2000). nia, 1978)butitis often useful to follow specific On the other, there is no conceptual objection case studies where temporal and spatial variabil- to theinability of McGowan and Walker (1985)to ity needed to be resolved statistically (Moll and demonstrate any significant variation in the rank- Rohlf, 1981). order of species abundances in the North Atlantic The second reason is the perspective that at spatial scales up to 800 km, despite strong is required for the ecological interpretation of small-scale spatial and interseasonal and inter- information on the structure and distribution of annual heterogeneity. This is attributable to the planktic communities in nature. This is crucial large-scale coherences in the basin-scale forcing to the ideas to be developed in subsequent chap- functions (direct measurements of the mid-depth ters of this book. It is not just a case of defining circulation of this part of the Atlantic Ocean the confidence intervals of quantitative deduc- have been given by Bower et al., 2002). Analogous tions about organisms whose distribution has relationships among planktic components have long been regarded as non-random, and over a been shown to be widespread through exten- wide range of scales (Cassie, 1959; McAlice, 1970). sive circulation provinces of the tropical and In order to sort out the multiple constraints on subtropical Atlantic Ocean (Finenko et al., 2003), theselection, succession and sequencing of natu- despite significant intracompartmental variabil- ralphytoplankton populations, it is always neces- ity in abundance and considerable intercompart- sary to distinguish the dynamic driver from the metal structural differences. The observations starting base. The assemblage that is observed in demonstrate the nature of the interaction of pop- agiveparcelofwaterat given place and at a ulation dynamics with the distinguishable move- given time is unrelated to the present conditions ments of the water masses in shaping the species but is the outcome of a myriad of processing con- structures of the pelagic. straints applying to a finite inoculum of individual organisms of historic and probably inexplica- ble provenance. 2.8 Summary In this chapter, the focus has spanned the dissipation of a fortuitous and localised recruit- The chapter explores the nature of the relation- ment of algae in a relatively small, shallow lake ship that phytoplankters have with the physi- through to the relative uniformity of the plank- cal properties of their environment. Water is a ton composition of an oceanic basin. The one may dense, non-compressible, relatively viscous fluid, depend upon the rapidity of growth in relation to having aberrent, non-linear tendencies to expand diffusivity (Reynolds et al., 1993a); the other upon and contract. The water masses of lakes and seas the extent of a single and possibly severe growth are subject to convection generated by solar heat- constraint over an extensive area of open ocean ing and, more especially, by cooling heat losses (Denman and Platt, 1975). Thus, it is important to from the surface. These motions are enhanced emphasise that although the entraining motions in the surface layers interfacing with the atmo- and horizontal diffusivity of pelagic water masses sphere, where frictional stresses impart mechan- influence profoundly the distribution of phyto- ical energy to the water through boundary-layer plankton, they do not confine organisms to a wave generation and frictional drag. Diel cycles fixed position in relation to the motion. Trans- of insolation, geographical variations in heat- port in the constrained circulation of a small lake ing and cooling, atmospheric pressure and the or passage in an open ocean current each sets amplifying inertia caused by the rotation of the abackground for the dynamics of change and Earth represent continuous but variable drivers variations in composition. The various outcomes of motion in aquatic environments. These can arising from differing relative contributions of rarely be regarded as still: water is continuously the same basic entraining processes are remark- in motion. However, the viscous resistance of the ably disparate. On the one hand, we can explain waterdetermines that the introduced motion SUMMARY 91 is damped and dissipated through a spectrum exceeded by u∗ by a factor of ≥15. Thus, the best of turbulent eddies of diminishing size, until descriptor of algal entrainability turns out to be molecular forces overwhelm the residual kinetic its sinking rate and, the greater is the adaptive energy. Instrumentation confirms emerging tur- ability to minimise it, the better able is the alga bulence theory about the extent of water layers to contribute to its persistence in an adequately subject to turbulent mixing and the sizes of the mixed water column. smallest eddies (generally around 1 mm), which, The adaptive mechanisms for lowering the together, most characterise the medium in which sinking velocity are reviewed in the context all pelagic organisms, and phytoplankton in par- of the Stokes equation and its various deriva- ticular, have to function. tives. Of the equation components, only parti- The most striking general conclusion is that cle size, particle density and particle form resis- most phytoplankters experience an immediate tance are considered subject to evolutionary or environment that is characteristically viscous. Yet behavioural adaptation. Examples of each adap- thephysical scale is such that individuals of most tation are quantified. Adaptations to control or categories of plankter (those less than 0.2 mm in offset density and the beneficial effects of distor- size) and their adjacent media are liable to be tion from the spherical form are demonstrated. transported wherever the characteristic motion The consequences of chain formation and cylin- determines. From the standpoint of the plank- drical elongation (into filaments) on sinking rate ter, the important criteria of the turbulent layer are explored and the effects of cell aggregation are its vertical extent (hm)andtherateatwhich to form the distinctive coenobia of Asterionella it dissipates its turbulent kinetic energy (E). Both and Fragilaria are evaluated. In relation to the are related to the intensity of the turbulence (u∗2) presumed vital regulatory component in sinking and, thus, to the turbulent velocity (u∗). rate, some possible mechanisms are discussed. The traditional supposition that the survival Some of the explanations offered are eliminated strategy of phytoplankton centres on an ability but there remain others that await careful inves- to minimise sinking is carefully updated in the tigation. context of pelagic motion. Extended residence Some larger, motile organisms are success- in the upper water layers remains the central ful plankters by virtue of adaptations that are requirement at most times. This is attained, in antithetical to increasing entrainability. Large, many instances, by maximising the entrainabil- motile species of Microcystis, Volvox, Ceratium and ity of the plankter within the motion. Viewed Peridinium combine relatively large size, motil- at a slightly larger scale, many phytoplankters ity and shape-streamlining to be able to escape optimise their ‘embedding’ within the surface moderate-to-low turbulent intensities in order to mixed layer. Criteria for plankter entrainment perform controlled migrations, at rates of several are considered – for it can only be complete if the metres per day. Reducing sinking rate is far from plankter has precisely the same density as (or is being a unique or universal adaptation qualify- isopycnic with) the suspending aqueous medium. ing microorganisms for a planktic existence. Even were this always desirable, it would be dif- In the later sections of the chapter, various ficult to attain. Not only does the water vary in types of behaviour are illustrated through spe- density with temperature and solute-content but cific examples of the vertical distributions of the components of phytoplankton cells are rather planktic algae in relation to the increased differ- more dense than water (typically amounting to entiation of density structure in the water col- 1020–1263 kg m−3, compared to <1000; Table 2.3). umn. The impacts are extrapolated to horizon- Following Humphries and Imberger (1982), rela- tal distribution and to the instances of small- tive entrainment ( )isinstead suggested to be scale patchiness and advective patchiness in governed by the relationship between particle small lakes, resolving in terms of algal migratory buoyancy and turbulent diffusivity. Effectively, in speeds in relation to the velocity of advective cur- order to achieve turbulent entrainment, an alga’s rents. The viability and persistence of phytoplank- sinking rate, ws (or its flotation rate, −ws)mustbe ton patches in expansive, large-scale systems, 92 ENTRAINMENT AND DISTRIBUTION IN THE PELAGIC

where return currents are extremely remote, ongoing or persistent rapid recuitment of organ- relate to the comparative rates of recruitment isms from point sources. within the patch and of the erosion at the patch Many different distributional outcomes can periphery. Some case studies are presented to be explained by the behaviour and dispersiveness show some very contrasted large-scale outcomes, of particular species in given systems, although distinguishing enduring community similarities the subjugated deployment of the same processes over 800 km in the horizontal from sharply elsewhere may contribute to the formation of localised patches in systems able to support quite different patterns. Chapter 3

Photosynthesis and carbon acquisition in phytoplankton

their energy by respiring (oxidising) the carbo- 3.1 Introduction hydrates and proteins manufactured (reduced) by photosynthesising plants, the presently per- The first aim of this chapter is to summarise the ceived realities of aquatic-reductant fluxes may biochemical basis of photosynthesis in planktic seem quite counter-intuitive. The original pos- algae and to review the physiological sensitivi- tulate is not in error: it succeeds in describ- ties of carbon fixation and assimilation under the ing how a section of the trophic relationships environmental conditions experienced by natu- of the pelagic is conducted. It is just that it is ral populations of phytoplankton. These funda- farfrom being the whole story. For instance, mental aspects of autotrophy are plainly rele- thephotosynthetic reduction of carbon is ante- vant to the dynamics and population ecology of dated by several hundreds of millions of years individual algal species, functioning within the (≥0.4 Ga: Falkowski, 2002)bythechemosynthe- constraints set by temperature and by the natu- sis by Archaeans of reduced carbon. This contin- ral fluxes of light energy and inorganic carbon. ues to be maintained in deep-ocean hydrother- They are also relevant to the function of entire mal vents, where there is no sunlight and only pelagic systems as, frequently, they furnish the minimal supplies of organic nutrients (Karl et al., major source of energy, in the form of reduced 1980; Jannasch and Mottl, 1985). Even in the carbon, to heterotrophic consumers. The yields of upper, illuminated waters of lakes and seas, most fish, birds and mammals in aquatic systems are (perhaps 60–95%) of the organic carbon present ultimately related to the harvestable and assimil- is not organismic but in solution (Sugimura and able sources of carbon bonds. In turn, the energy Suzuki, 1988;Wetzel, 1995; Thomas, 1997). A and resource fluxes through the entire biosphere large proportion of this is humic in character are greatly influenced by pelagic primary produc- and, thus, supposed to be derived from terres- ers, impinging on the gaseous composition of the trial soils and ecosystems. True, much of this car- atmosphere and the heat balance of the whole bon would have been reduced orginally through planet. terrestrial photosynthesis but the extent of its Here, we shall be concerned with events at contribution to the assembly of marine biomass the population, community and ecosystem lev- is still not fully clear. Setting this aside, the els. However, it is necessary to emphasise at direct phagotrophic transfer of photosynthetic the start of thechapterthat recent advances primary products from phytoplankton to zoo- in understanding of planetary carbon stores and planktic consumers is not universally achieved fluxes assist our appreciation of the relative in the pelagic but is, in fact, commonly mediated global importance of aquatic photosynthesis. To by the activities of free-living microbes. Thus, the those biologists of my generation brought up dynamic relationships among phytoplankton and with the exclusive axiom that animals derive their potential phagotrophic consumers acquire 94 PHOTOSYNTHESIS AND CARBON ACQUISITION

anew interpretative significance, which is to be been overtaken by new information. At the same addressed in this and later chapters. time, it is possible to predict that future progress The present chapter prepares some of the will concern the biochemical and biophysical ground necessary to understanding the relation intricacies of control and regulation more than of planktic photoautotrophy to the dynamics thebroad principles of process and order-of- of phytoplankton populations. After considering magnitude yields, which are generally accepted the biochemical and physiological basis of photo- by physiological ecologists. Thus, the contempor- synthetic production, the chapter compares the ary biochemical basis for assessing phytoplankton various limitations on the assembly of photoau- production will continue to be valid for some totrophic biomass in natural lakes and seas, and time to come. it considers the implications for species selection Photosynthesis comprises a series of reac- and assemblage composition. tions that involve the absorption of light quanta (photons); the deployment of power to the reduction of water molecules and the release of 3.2 Essential biochemistry of oxygen; and the capture of the liberated electrons in the synthesis of energy-conserving com- photosynthesis pounds, which are used ultimately in the Calvin cycle of carbon-dioxide carboxylation to form It has been stated or implied several times already hexose (Falkowski and Raven, 1997;Geider and that the paramount requirement of photoau- MacIntyre, 2002). The aggregate of these reac- totrophic plankton to prolong residence in, or tions may be summarised: gain frequent access to, the upper, illuminated H O + CO + photons = 1/6[C H O ] + O (3.1) layers of the pelagic is consequential upon the 2 2 6 12 6 2 requirement for light. The need to capture solar As with most summaries, Eq. (3.1)omits not energy in order to drive photosynthetic carbon merely detail but several important intermedi- fixation and anabolic growth is no different ate feedback switches, involving carbon, oxy- from that experienced by any other chlorophyll- genand reductant, all of which have a bear- containing photoautotroph inhabiting the suring upon the output products and their physio- face of the Earth. Indeed, the mechanisms and logical allocation in active phytoplankters. These ultrastructural provisions for bringing this about are best appreciated against the background constitutes one of the most universally conserved of the supposed ‘normal pathway’ of photosyn- processes amongst all photoautotrophic organ- thetic electron transport. The latter was famously isms. On the other hand, to achieve, within the proposed by Hill and Bendall (1960). Their z- bounds of an effectively opaque and fluid envi- model of two, linked redox gradients (photo- ronment, a net excess of energy harvested over systems) has been well substantiated, biochemi- the energy consumed in metabolism requires cer- cally and ultrastructurally. In the first of these tain features of photosynthetic production that (perversely, still referred to as photosystem II, are peculiar to the plankton. Thus, our approach or PSII), electrons are stripped, ultimately from should be to rehearse the fundamental require- water, and transported to a reductant pool. ments and sensitivities of photosynthetic produc- In the second (photosystem I, or PSI), photon tion and then seek to review the aspects of the energy is used to re-elevate the electrochemical pelagic lifestyle that constrain their adaptation potential sufficiently to transfer electrons to car- and govern their yields. bon dioxide, through the reduction of nicoti- Enormous strides in photosynthetic chem- namide adenine dinuceotide phosphate (NADP to istry have been made, especially over the last NADPH). 30 years or so, especially at the molecular and The (Calvin cycle) carbon reduction is based submolecular levels (Barber and Anderson, 2002). on the carboxylation reaction. Catalysed by ribu- This progress is not likely to stop so that, undou- lose 1,5-biphosphate carboxylase (RUBISCO), one btedly, whatever is written here will have soon molecule each of carbon dioxide, water and ESSENTIAL BIOCHEMISTRY OF PHOTOSYNTHESIS 95 ribulose 1,5-biphosphate (RuBP) react to yield two 46–48% of the total quantum flux. The corre- molecules of the initial fixation product, glycer- sponding photon flux density averages 1.77 × ate 3-phosphate (G3P). This latter reacts with ATP 1021 m−2 s−1.Division by the Avogadro num- and NADPH to form the sugar precursor, glycer- ber (1 mol = 6.023 × 1023 photons) expresses aldehyde 3-phosphate (GA3P), which now incor- the maximum flux in the more customary porates the high energy phosphate bond. In the units, einsteins or mols, 2.94 mmol photon remaining steps of the Calvin cycle, GA3P is fur- m−2 s−1. The energy of a single photon, ´ε,varies ther metabolised, first to triose, then to hexose, with the wavelength, and RuBP is regenerated. ´ε = hc/λ (3.2) At themolecular level, photosynthetic reactivity is plainly sensitive to the supply of carbon and where h is Planck’s constant, having the value water, the photon harvesting and, like all other 6.63 × 10−34 Js (e.g. Kirk, 1994). Photons at the biochemical processes, to the ambient tempera- red end of the PAR spectrum each contain about ture. Measurement of photosynthesis may invoke 2.84 × 10−19 J, about 57% of the content of blue- ayield of fixed carbon, the quantum efficiency light photons (4.97 × 10−19 J). of its synthesis (yield per photon), or the amount While a given radiation flux of light of a of oxygen liberated. None of these is any longer single wavelength can be readily expressed in difficult to quantify but the difficulty is still the Js−1 (and vice versa), precise conversion across correct interpretation of the bulk results. It is aspectral band does not apply. The approximate still necessary to consider carefully the regula- relationship proposed by Morel and Smith (1974) tory role of the ultrastructural and biochemical forthe interconversion of solar radiation in the components that govern the photosynthesis of 400–700 nm band of 2.77 × 1018 quanta s−1 W−1 phytoplankton. Special attention is directed to (equivalent to 3.62 × 10−19 Jperphoton, or 218 kJ the issues ofphoton harvesting, the internal elec- per mol photon) has general applicability (Kirk, tron transfer, carbon uptake, RUBISCO activity 1994). and the behaviour of the regulatory safeguards Photosynthesis depends upon the intercep- that phytoplankters invoke in order to function tion and absorption of photons. Both photosys- in highly variable environments. tems involve the photosynthetic pigment chlorophyll a (and, where applicable, other chloro- 3.2.1 Light harvesting, excitation and phylls), which is characteristically complexed electron capture with particular proteins, and certain other pig- Light is the visible part of the spectrum of ments in many instances. These are accom- electromagnetic radiation emanating from the modated within structures known as light- sun. Electromagnetic energy occurs in indivisi- harvesting complexes (LHC) and it is these that ble units, called quanta, that travel along sinu- act as antennae in picking up incoming pho- soidal trajectories, at a velocity (in air) of c ∼ 3 × tons. For instance, the light-harvesting complex 108 ms−1. The wavelengths of the quanta define of the eukaryotic photochemical system II (LHCII) their properties – those with wavelengths (λ) typically comprises some 200–300 chlorophyll between 400 and 700 nm (400 – 700 × 10−9 m) molecules (mostly of chlorophyll a;upto30% correspond with the visible wavelengths we call may be of chlorophyll b), the specific chlorophyll- light (and within which waveband the quanta are binding proteins and a variable number of xan- called photons). The waveband of photosynthetically thophyll and carotene molecules, to a combined active radiation (PAR) coincides almost exactly with molecular mass of 300–400 kDa (Dau, 1994;Gous- that of light. The white light of the visible spec- sias et al., 2002). The prokaryotic Cyanobacte- trum is the aggregate of the flux of photons of ria lack chlorophyll b and the light-harvesting differing wavelengths, ranging from the shorter chlorophyll-proteins of PSII. They rely instead (blue) to the longer (red) parts of the spectrum. on the phycobiliproteins, assembled in bodies Relative to the solar constant (see Sec- known as phycobilisomes (Grossman et al., 1993; tion 2.2.2), the PAR waveband represents some Rudiger,¨ 1994). 96 PHOTOSYNTHESIS AND CARBON ACQUISITION

At the heart of the eukaryote LHCII is the chlorophyll-protein complex (known as P700)and antennal chlorophyll-protein known as P680.Itis acceptor (usually denoted A). Again, photons here that the reactions of PSII are initiated, when excite the equivalent number of P700 electrons to the complex is exposed to light. The energy of a thepoint where they can be accepted by A. Next single photon is sufficient to raise a P680 electron in the electron transfer pathway is ferredoxin, from its ground-state to its excited-state orbital. transfer of electrons to which reoxidises A− while Next to the P680 is the phaeophytin acceptor donation of the equivalent number from the plas- molecule (usually referred to as ‘Phaeo’) and the toquinone pool re-reduces P700 molecules. The two further acceptor quinones (Q A and Q B)that electrons may be passed from ferredoxin, and comprise the PSII reaction centre. In sequence, beyond PSI, to bring about the reduction of NADP this acceptor chain passes the electrons to PSI. to NADPH that provides power to drive Calvin- + The reaction (P680 → P680 )isoneofthemost cycle carboxylation. The subsequent reactions of powerful biological oxidations known to science; NADPH with carbon dioxide are not directly the electrons are readily captured by the Phaeo dependent upon the photon flux and can con- acceptor. In its now-reduced state, Phaeo− in turn tinue in darkness (see Section 3.2.3). − activates the Q A acceptor: its reduction to Q A The PSI generation of the carbon-reducing stimulates acceptance of the electron by Q B. power nevertheless also requires the photosyn- In this way, the electrons are serially trans- thetic transfer of four electrons per atom of car- ported towards PSI. Once it has accepted two elec- bon. Under ideal conditions, the light reactions trons, Q B dissociates to enter a pool of reduced in photosynthesis may be summarised: plastoquinone (‘PQ’). Molecules of PQH2 are even- 2NADP + 3ADP + 3P + 2H2O + 8e tually oxidised by the cytochrome known as b6/f, → + + + + + which carries the electrons to PSI. 2NADPH 3ATP 3P 2H O2 (3.3) The plastoquinone pool functions as a system capacitor, like a sort of surge tank of reductant 3.2.2 Photosystem architecture (D. Walker, 1992;KolberandFalkowski, 1993), The electron transfer that this equation repre- whose activity can be viewed in the context of sents is readily facilitated by the physical arrange- PSII light harvesting. At quiescence, the entire ment of the two main components (PSII, PSI) reaction centre is said to be ‘open’: P680 is in its and the intercoupling plastoquinone pool, the reduced state, Phaeo and QA are oxidised. Then, b6/f cytochrome complex and, in most algae photon excitation of the P680 initiates a flow of and plants, the soluble electron carrier plasto- electrons to the plastoquinine pool, whence they cyanin (in Cyanobacteria, cytochrome c may sub- may be removed as rapidly as PSI can accept stitute). The basic architecture and the location them. At the same time, the otherwise uncomple- of the biochemical functions of the photosyn- + mented positive charge of excited P680 is balanced thetic units seems to be extremely well conserved by the stripping of electrons from water (that among eukaryotic algae, plants and their ances- + is, P680 is reduced back to P680). Note that four tral cyanobacterial lines. The best-known features photochemical reactions are necessary to gener- were revealed long ago, through light microscopy ate one dioxygen molecule from two molecules and early transmission electron microscopy. The + of water (2H2O → 4H + 4e + O2). It is now granule-like units, comprising LHC antennae and + understood that P680 is actually reduced through thereaction centres, are strung on proteinaceous the action of manganese ions, via a redox-active membranes, called thylakoids. In the cells of tyrosine (Barber and Nield, 2002). However, until eukaryotes, stacks of thylakoids are contained + the P680 molecule is re-reduced, the reaction cen- within one or more separate membrane-bound tre is unable to accept further electrons and it envelopes, the chromophores (also called plastids is said to be ‘closed’. It remains so until Q A is or, where they occur in chlorophyte algae and reoxidised. all higher plants, chloroplasts) whose shape and The light-harvesting complex and reaction arrangement is often taxon-specific. Cyanobacte- centre of PSI are built around an analogous ria lack separate chromophores; the thylakoids ESSENTIAL BIOCHEMISTRY OF PHOTOSYNTHESIS 97

Figure 3.1 Diagram of the configuration of the structure and the flow of excitation energy through the photsystems. Electrons are extracted from water in photosystem II and transported through the quinone cycle and released to photosystem I. Electrons are accepted by ferredoxin, to bring about the reduction of NADP to NADPH that enables the cell to synthesise its molecular components. Redrawn, with permission from Kühlbrandt (2001). are rather loosely dispersed through the body of and, equally, its reactions to damagingly high the cell. Apart from anchoring the various trans- light levels. The relevant ultrastructural and bio- membrane structures (including, in the case of chemical input parameters concern how much the Cyanobacteria, the phycobilisomes), the thy- light-harvesting capacity there is present in an lakoid also maintains a regulatory charge gradi- alga and how much reductant it can deliver per ent, down which the electrons are passed. unit time. The molecular structure of the energy- The arrangement and linkage of the photo- harvesting apparatus has become clearer as a systems are schematised in Fig. 3.1. The size of result of the recent application of electron crys- the LHCII structures studied by Kuhlbrandt¨ et al. tallography. Since Kuhlbrandt¨ and Wang (1991) (1994)averaged13nminareaand4.8nminthick- published the three-dimensional structure of ness. The PSII complexes from Synechococcus mea- alight-harvesting complex, other investigative sured roughly 19 × 10 nm across and 12 nm thick studies have followed, showing, at increasingly (Zouni et al., 2001). The LHCI complexes from Syne- fine resolution, the organisation and interlink- chococcus revealed by Jordan et al. (2001)areappar- ages of the major sub-units ofPSIIinplantsand ently of similar size. On the basis of there being Cyanobacteria (McDermott et al., 1995;Zouni et 200–300 chlorophyll molecules in a typical LHC, al., 2001;Barberand Nield, 2002)andalso of Reynolds (1997a) calculated that 1 g chlorophyll PSI (Jordan et al., 2001). The recent overview and could be organised into 2.2 to 3.4 × 1018 LHCs. model of Fromme et al.(2002)upholds that pro- Because the area that1gofchlorophyllsubtends posed by Kuhlbrandt¨ et al.(1994)andupdates it in the light field can be as great as 20 m2 (see in several respects. Section 3.3.3), each LHC contributes an average The cited literature should be consulted for photon absorption of up to 10 × 10−18 m−2 (i.e. more of the fascinating details of the struc- 10 nm2). tures and organisational patterns of light har- It was also supposed that the photon absorp- vesting and the electron-transport chain. Here, tion is in inverse proportion to the product of the we should emphasise the generalised configura- area of the LHC and the aggregate time for the tion and functional dynamics of the various sub- electron transport chain to accept photons and units involved in photon absorption and electron clear electrons, ready for the next photon. Kolber capture, for it is these which impinge upon their and Falkowski (1993) approximated the aggregate physiological performance and their adaptability time of reactions linking initial excitation (occu- to operation under sub-ideal conditions. As will pying lessthan100fs, or 10−13: Knox, 1977)tothe − be seen (in Section 3.3), the relevant outputs of re-oxidation of Q A to be 0.6 ms. The principal rate- an adequate carbon-reducing capacity relate to limiting step is the onward passage of electrons system performance under ambient light fluxes, from the plastoquinone pool, which, depending how it behaves in poor light (low photon fluxes) upon temperature, needed between 2 and 15 ms. 98 PHOTOSYNTHESIS AND CARBON ACQUISITION

Thus, a single pathway might accommodate up to 66 reactions per second at 0 ◦Candsome 500 s−1 at 30 ◦C, with a matching carbon-reducing power. As a rough approximation indicates that, at 30 ◦C, 1 g chlorophyll containing >2 × 1018 active LHCs has the capacity to deliver >1021 electrons every second and a theoretical potential to reduce more than 1.25 × 1020 atoms of carbon [i.e. > ∼200 µmolC(gchla)−1 s−1].

3.2.3 Carbon reduction and allocation As noted above, the fixation of carbon dioxide occurs downstream of the energy capture, where the reducing power inherent in NADPH is deployed in the synthesis of carbohydrate. The flow of reductant drives the Calvin cycle of RuBP consumption and regeneration, during which carbon dioxide is drawn in and glucose is discharged. The cycle is summarised in Fig. 3.2.In Figure 3.2 The Calvin cycle. Carboxylation by RUBISCO thealgae and in many higher plants, RUBISCO- of RuBP at 1 is driven by ATP and NADPH generated by the mediated carboxylation of RuBP yields the first light reactions of photosynthesis, and results ultimately in the synthesis of sugar precursors and the renewed availability of stable product of so-called C3 photosynthetic carbon fixation, the 3-carbon glycerate 3-phosphate RuBP substrate, thus maintaining the cycle. The cycle is regulated at the numbered reactions, where it may be (G3P). (Note that in this, the process differs from short-circuited as shown. Abbreviations: DHAP, those terrestrial C4 fixers that synthesise four- dihydroxyaceton phosphate; E4P, erythrose 4-phosphate; FBP, carbon malate or aspartate.) fructose 1,5-biphosphate; F6P, fructose 6-phosphate; GA3P, After the further NADPH-reduction of G3P glyceraldehyde 3-phosphate; GBP, glycerate 1,3-biphosphate; to glyceraldehyde 3-phosphate (GA3P), the G3P, glycerate 3-phosphate; G6P, glucose 6-phosphate; Pi, metabolism proceeds through a series of sugar- inorganic phosphate; RuBP, ribulose 1,5-biphospharte; Ru5P, phosphate intermediates to yield a hexose ribulose 5-phosphate; R5P, ribose 5-phospate; SBP, (usually glucose). In this way, one molecule of sedoheptulose 1,7-biphosphate; S7P, sedoheptulose hexose may be exported from the Calvin cycle 7-phosphate; Xu5P, xylulose 5-phosphate. Redrawn with permission from Geider and MacIntyre (2002). for every fiveofGA3Preturnedtothecycle of RuBP regeneration and, ideally, one for every six molecules of carbon dioxide imported. In this case of steady-state photosynthesis, the following way, theoverall photosynthetic Eq. (3.1)isbal- equation summarises the mass balance through anced, at the minimal energy cost of eight pho- the Calvin cycle: tons per atom of carbon fixed. Thus, the theoretical maximum quantum yield of photosynthesis (ϕ)is + + + + − CO2 2NADPH 3ATP 2H 0.125 mol C (mol photon) 1 (D. Walker, 1992).

→ 1/6C6H12O6 + H2O + 2NADP However, neither the cycle nor its fixed-carbon + 3ADP + 3P (3.4) yield is immutable but it is subject to deviation and to autoregulation, according to circum- According to demand, the glucose may be stances. As stated at the outset, these have rever- respired immediately to fuel the energy demands berations at successive levels of cell growth, com- of metabolism, or it may be submitted to the munity composition, ecosystem function and the amination reactions leading to protein synthe- geochemistry of the biosphere. The variability sis. Excesses may be polymerised into polysac- may owe to imbalances in the light harvest and charides (glycogen, starch, paramylon). In this carbon capture, or to difficulties in allocating ESSENTIAL BIOCHEMISTRY OF PHOTOSYNTHESIS 99 the carbon fixed. To evaluate these resourcing adequate intracellular carbon supply and upon impacts requires us to look again at the sensitiv- theRUBISCO capacity or, at least, upon that ity of the Calvin-cycle reactions, beginning with proportion of RUBISCO capacity that is actually theinitial carboxylation and the action of the ‘active’. To be catalytcally competent, the active RUBISCO enzyme. site of RUBISCO has also to be carbamylated by RUBISCO, the catalyst of the CO2–RuBP con- thebinding of a magnesium ion and a non- junction, is a most highly conserved enzyme, substrate CO2 molecule. Under low light and/or occurring, with little variation, throughout the low carbon availability, RUBISCO is inactivated photosynthetic carbon-fixers (Geider and Mac- (decarbamylated), by the reversible action of an Intyre, 2002). From the bacteria, through the enzyme (appropriately known as RUBISCO inac- ‘red line’ and the ‘green line’ of algae (see tivase), to match the slower rate of RuBP regen- Section 1.3), to the seed-bearing angiosperms, eration. The resultant down-cycle sequestration present-day photosynthetic organisms have to of phosphate ions and lower ATP regeneration contend with acknowledged catalytical weak- brings about an increase in ADP : ATP ratio and, nesses of RUBISCO. These are due, in part, to thus, a decrease in RUBISCO activity (for fur- the fact that carbon-dioxide-based photosynthesis ther details of Calvin-cycle self-regulation, refer evolved under different atmospheric conditions to Geider and MacIntyre, 2002). from those that presently obtain. In particular, The action of RUBISCO inactivase is itself sen- the progressive decline in the partial pressure of sitive to the ADP : ATP ratio and to the redox CO2 exposes the rather weak affinity of RUBISCO state of PSI. Thus, RUBISCO activity responds pos- for CO2 (Tortell, 2000). According to Raven (1997), itively to a cue of a light-stimulated accelera- the maximum reported rates of carboxylation (80 tion in photosynthetic electron flow. With con- −1 −1 mol CO2 (mol RUBISCO) s :Geider and MacIn- ditions of high-light-driven reductant fluxes and tyre, 2002)are low compared to those mediated high CO2 availability at the sites of carboxylation, by other carboxylases. Even these levels of activ- thelimitation of photosynthetic rate switches to ity are dependent upon a significant concentra- the rateofRuBP complexation and renewal, both tion of carbon dioxide at the reaction site (with of which become subject to the overriding con- reported half-saturation constants of 12–60 µM straint of the RUBISCO capacity (Tortell, 2000). among eukaryotic algae: Badger et al., 1998). Sup- However, the kinetics of RUBISCO activity impose posing that the cell-specific rate of carbon fixa- a heavy demand in terms of the delivery of car- tion could be raised by elevating the amount of bon dioxide to the carboxylation sites. Although active RUBISCO available, the investment in its many phytoplankters invoke biophysical mecha- large molecule (∼560 kDa) is relatively expensive. nisms for concentrating carbon dioxide (see Sec- RUBISCO may account for 1–10% of cell carbon tion 3.4), the relatively high levels needed to satu- and 2–10% of its protein (Geider and MacIntyre, rate the carboxylation function of RUBISCO may 2002). frequently be overtaken. Circumstances that com- Having more RUBISCO capacity is not nec- bine low CO2 with the high rates of reductant essarily helpful either, owing to the susceptibil- and oxygen generation possible in strong light ity of RUBISCO to oxygen inhibition: at low CO2 are liable to effect the competitive switch to the concentrations (<10 µM) and high O2 concentra- oxygenase function of RUBISCO and the incep- tions (>400 µM), RUBISCO functions as an oxi- tion of photorespiration. dase, in initiating an alternative reaction that Photorespiration is a term introduced in the leads to the formation of glycerate 3-phosphate physiology of vascular plants to refer to the and phosphoglycolate. In the steady-state Calvin- sequence of reactions that commence with the cycle operation, the activity of RUBISCO serves formation of phosphoglycolate from the oxygena- to maintain the balance between NADPH gen- tion of RuBP by RUBISCO (Osmond, 1981). In the eration and the output of carbohydrates. For a present context, the term covers the metabolism given supply of reductant from PSI, the rate of of reductant power and controlling photosynthe- carbon fixation may be seen to depend upon an sis at low CO2 concentrations. The manufacture 100 PHOTOSYNTHESIS AND CARBON ACQUISITION

of phosphglycolate carries a significant energetic yields and the energetic efficiency of photosyn- cost through the altered ATP balance (see Raven thetic carbon fixation. The basic equation (3.1) et al., 2000), though this is partly recouped in indicates equimolecular exchanges between car- the continued (albeit smaller) RUBISCO-mediated bon dioxide consumed and oxygen released (the contribution of G3P to the Calvin cycle. Mean- photosynthetic quotient, PQ, mol O2 evolved/mol while, the phosphoglycolate is itself dephos- CO2 assimilated, is 1). In fact, both components phorylated (by phosphoglycolate phosphatase) to are subject to partially independent variation. form glycolic acid. In the ‘green line’ of algae Oxygen cycling may occur within the photosyn- (including the prasinophytes, chlorophytes and thetis electron transfer chain (the Mehler reac- euglenophytes) and higher plants, this glycolate tion), independently of the amount of carbon can be further oxidised, to glyoxalate and thence delivered through the system. The ‘competition’ to G3P. The full sequence of reactions has been between the carboxylation and oxidation activ- called the ‘photosynthetic carbon oxidation cycle’ ity of RUBISCO are swayed in favour of oxy- (PCOC) (Raven, 1997). In the Cyanobacteria and in genproduction, photorespiration and glycolate the‘red line’ of algae, this capacity seems to be metabolism (Geider and MacIntyre, 2002). The PQ generally lacking. When experiencing oxidative may move from close to 1.0 in normally photo- stress at high irradiance levels, these organisms synthesising cells (actually, it is generally mea- cells will excrete glycolate into the medium. sured to be 1.1 to 1.2: Kirk, 1994)totherange Excreted glycolate is sufficiently conspicuous 1.2 to1.8under high rates of carbon-limited outside affected cells for its production to have photosynthesis. Low photosynthetic rates under been studied for many years as a principal ‘extra- high partial pressures of oxygen may force cellular product’ of phytoplankton photosynthe- PQ < 1 (Burris, 1981). sis (Fogg, 1971). It is now known that not only The effects on energy efficiency are also sensi- glycolate but also other photosynthetic interme- tive to biochemical flexibility. Taking glucose as diates and soluble anabolic products are released an example, the energy stored and released in the from cells into the medium. This apparent squan- complete oxidation of its molecule is equivalent dering of costly, autogenic products seemed to to 2.821 kJ mol−1,or∼470 kJ per mol carbon syn- be an unlikely activity in which ‘healthy’ cells thesised. The electron stoichiometry of the syn- might engage (cf. Sharp, 1977). However, it is thesis cannot be less than 8 mol photon (mol now appreciated that, far from being a conse- C)−1 but, energetically, the photon efficiency is quence of ill health, the venting of unusable dis- weaker. The interconversion of Morel and Smith solved organic carbon (DOC) into the medium (1974;see above; 1 mol photon ∼218kJ) implies constitutes a vital aspect of the cell’s homeo- an average investment of the energy of 12.94 pho- static maintenance (Reynolds, 1997a). It is espe- tons mol−1. This coincides more closely to the cially important, for example, when the pro- highest quantum yields determined experimen- ducer cells are unable to match other growth- tally (0.07–0.09 mol C per mol photon: Bannister sustaining materials to the synthesis of the carbo- and Weidemann, 1984;D.Walker, 1992). hydrate base. In natural environments, the DOC Clearly, even these yields are subject to compounds thus released – glycolate, monosac- thevariability in the fate of primary photo- charides, carboxylic acid, amino acids (Sorokin, synthate. Moreover, the alternative allocations 1999,p.64;seealsoGroverandChrzanowski, of the fixed carbon (whether polymerised and 2000; Søndergaard et al., 2000)–are readily taken stored, respired, allocated to protein synthesis or up and metabolised by pelagic microorganisms. excreted) need to be borne in mind. It is well The far-reaching ecological consequences of this accepted that about half the photosynthate in behaviour are explored in later sections of this actively growing, nutrient-replete cells is invested book (Sections 3.5.4, 8.2.1). in protein synthesis and in the replication of So far as the biochemistry of photosynthesis cell material (Li and Platt, 1982;Reynoldset al., is concerned, these alternative sinks for primary 1985). However, this proportion is very suscepti- product make it less easy to be precise about the ble to the physiological stresses experienced by LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 101 plankters in their natural environments as a con- adopted until it had been described in English sequence of low light incomes, carbon deficien- (Gaarder and Gran, 1927). Although it was pos- cies or severe nutrient depletion. These effects sible at that time to estimate carbon dioxide are explored in subsequent sections. uptake in similar bottles, essentially through the use of pH-sensitive indicator dyes, the measurement of photosynthetic rate through changes in 3.3 Light-dependent environmental oxygen concentration in light and dark bottles wassoon adopted as a standard method in bio- sensitivity of photosynthesis logical limnology and oceanography.

In this section, the focus moves towards the 3.3.1 Measurement of light-dependent physiology of photosynthetic behaviour of phy- photosynthetic oxygen production toplankton in natural lakes and seas, especially Numerous studies based on oxygen generation its relationship with underwater light availabil- in light and darkened bottles were published ity. According to a recently compiled history of in the 50 years between 1935 and 1985. Many phytoplankton productivity (Barber and Hilting, of the findings were substantially covered in a 2002), quantification of pelagic photosynthesis thorough synthesis by Harris (1978). Since then, developed through a series of sharp conceptual themethod has been displaced by more direct and (especially) methodological jumps. After a and more sensitive techniques. Nevertheless, the rapid series of discoveries in the late eighteenth experiments based on measurements of photo- century, establishing that plants need light and synthetic oxygen production in closed bottles sus- carbon dioxide to produce oxygen and organic pended at selected depths in the water column matter from carbon dioxide, there was much yielded consistent generalised results and have slower progress in estimating the rates and mag- bequeathed to plankton science many of the con- nitude of the exchanges. This is especially true ceptual aspects and quantitative descriptors of foraquatic primary production, until the idea productive capacity. The set of sample results that it could have much bearing on the tropho- illustrated in Fig. 3.3 depicts a typical depth pro- dynamics of the sea became a matter of serious file of photosynthetic (4-h) exposures of unmodi- debate (see Section 1.2). It was not until the begin- fied lake plankton in relation to the underwater ning of the twentieth century, as concerns came light field in an unstratified temperate lake in to focus increasingly on the rates of reproduction winter (temperature ∼5 ◦C). The features of gen- and consumption of planktic food plants, that eral interest include the following: thepressing need for quantitative measures of r plankton production was identified (Gran, 1912). The plot of gross photosynthetic oxygen genera- Building on the techniques and observations of tion is shown as a function of depth in Fig. 3.3a. Whipple (1899), who had shown a light depen- The curve is fitted by eye. However, it is plain dence of the growth of phytoplankton in closed that photosynthesis over the 4 hours peaks a lit- bottles suspended at various depths of water, and tle way beneath the surface, with slower rates using the Winkler (1888)back-titration method being detected at depth. In this instance, as in for estimating dissolved oxygen concentration, alargenumber of other similar experiments, Gran and colleagues devised a method of mea- there is an apparent depression in photosyn- suring the photosynthetic evolution of oxygen in thetic rate towards the surface. r sealed bottles of natural phytoplankton, within The ‘gross photosynthesis’ is the measured measured time periods. Darkened bottles were aggregate oxygen production at a given depth set up to provide controls for respirational con- averaged over the exposure period. It is cal- sumption. They published (in 1918) the results of culated as the observed increase in oxygen astudy of photosynthesis carried out in the Chris- concentration in the ‘light’ bottle (usually a tiania Fjord (now Oslofjord). According to Barber mean of duplicates) plus the observed decrease and Hilting (2002), the method was not widely in concentration in the corresponding ‘dark’ 102 PHOTOSYNTHESIS AND CARBON ACQUISITION

r Figure 3.3 Specimen depth distributions of (a) total gross It was neither essential nor common to calcu- photosynthetic rate (NP) and total gross respiration rate late the respiratory uptake, as the depletion (NR); (b) the photosynthetic population (N), in terms of of oxygen concentration in the dark controls. chlorophyll a; (c) chlorophyll-specific photosynthetic rate (P All that was necessary was the additional mea- = NP/N) and respiration rate (R = NR/N); (d) underwater surement of the initial oxygen concentration irradiance (I)ineach of three spectral blocks, expressed as a at the start of the experiment. The change in percentage of the irradiance I obtaining immediately beneath 0 the dark bottles over the course of the exper- the surface. P is replotted against I, either (e) as a percentage iment, normalised to the base period, is the of I 0 in th green spectral block (peak: 530 nm), or as the reworked estimate of the intensity of the visible light above equivalent to the respiration of the enclosed the water (in µmol photon m−2 s−1)averaged through the organisms in the dark, NR (here, expressed in −3 −1 exposure period. Original data of the author, redrawn from mg O2 m h ); R (=NR/N)isthus supposed Reynolds (1984a). to be the biomass-specific respiration rate (in −1 −1 mg O2 consumed (mg chla) h ) inserted in control, it being supposed that the respiration Fig. 3.3c. However, the extrapolation must be in the dark applies equally to the similar mate- applied cautiously. Whereas NP,asdetermined, rial in the light. The mean gross photosyn- is attributable to photosynthesis, the separate thetic rate at the given depth (here, expressed determination of NR does not exclude respira- −3 −1 in mg O2 m h )represents NP,the product tion by non-photosynthetic organisms, includ- of a biomass-specific rate of photosynthesis (P, ing bacteria and zooplankton. Moreover, it can- −1 −1 here in mg O2 (mg chla) h )andthebiomass not be assumed that even basal respiration present (N,shown in Fig 3.3bandexpressed as rate of phytoplankton is identical in light and the amount of chlorophyll a in the enclosed darkness: according to Geider and MacIntyre plankton, in (mg chla)m−3). At this stage, it is (2002), oxygen consumption in photosynthesis- the biomass specific behaviour that is of first ing microflagellates is 3- to 20- (mean: 7-) fold interest: P (=NP/N)isplotted in Fig. 3.3c. The greater than dark respiration rate. Accelerated shape of the curve of P is scarcely distorted metabolism and excretion of photosynthate in from that of NP in this instance, owing to the starved or stressed phytoplankton may, con- uniformity of N with depth. Discontinuities in ceivably, account for all the materials fixed in the depth distribution of N do affect the shape photosynthesis: (P−R)issmall but dark R need of the NP plot (see below and Fig. 3.4). not be large either. LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 103

Figure 3.4 Some variations in the basic form of depth proﬁles of gross (NP) and chlorophyll-speciﬁc rates (P), explained in the text.

r The decline in biomass-specific P below the sub- (I430 + I530 + I630)z/3, and taking the immedi- surface maximum (Pmax)issupposedtobea ate subsurface irradiance (I0)astheaverage over function of the underwater extinction. In the theexperiment (in this instance, I0 = 800 µmol present example, the underwater light attenua- photons m−2 s−1). tion measured photometrically in each of three spectral bands of visible light (blue, absorption This last plot, Fig. 3.3f, conforms to the for- peaking at 430 nm; green, peaking at 530 nm; mat of the generic P vs. I curve. It has a steeply and red, peaking at 630 nm) is included as Fig. rising portion, in which P increases in direct pro- 3.3d. Note that the spectral balance changes portion to Iz;the slope of this line, generally with depth (blue light being absorbed faster notated as α (=P/Iz), is a measure of photosyn- than red or green light in this case). thetic efficiency at low light intensities. Express- r −1 −1 Replotting the biomass-specific rates of P ing P in mg O2 (mg chla) h and Iz in mol pho- −2 −1 against Iz,the level of the residual light pen- tons m h ,theslope, α, has the dimensions etrating to each of the depths of measurement of photosynthetic rate per unit of irradiance, mg −1 −1 (expressed as a percentage of the surface mea- O2 (mg chla) (mol photon) .Asthe incident surement), gives the new curve shown in Fig. photon flux is increased, P becomes increasingly 3.3e. This emphasises the sensitivity of P to Iz, less light dependent and, so, increasingly satu- at least at low percentage residual light pene- ratedbythe light available. The irradiance level tration, and a much more plateau-like feature representing the onset of light saturation is judged around P . to occur at the point of intersection between the r max Finally, the P vs. I curve is replotted in Fig. extrapolation of the linear light-dependent part 3.3finterms of the depth-dependent irradiance of the P − Iz curve with the back projection of across the spectrum, approximated from Iz = Pmax, being the fastest, light-independent rate of 104 PHOTOSYNTHESIS AND CARBON ACQUISITION

photosynthesis measured. This intensity, known growth and replication. In none of the experi- as Ik, can be judged by eye or, better, calculated ments considered by Gran (1912), nor those car- as: ried out half a century later by Lund (1949)or Reynolds (1973a), is there any question that the I = P /α mol photons m−2 h−1 (3.5) k max fastest population growth rates are obtained clos- It is usual (because that is how the photon flux is est to the water surface. In the late 1970s, some measured) to give light intensities in µmol pho- helpful experimental evidence was gathered to tons m−2 s−1.Intermsofbeing able to explain show that the surface depression was largely an the shape of the original P vs. depth curve (Fig. artefact of the method and the duration of its 3.3a), it is also useful to be able to define the application. Taking phytoplankton from a mixed water column and holding them steady at super- point in the water column, z(Ik) , where the rate of photosynthesis is directly dependent on the saturating light intensities for hours on end rep- photon flux. The left-hand, light-limited part of resents an enforced ‘shock’ or ‘stress’. In these the P vs. Iz curve is the most useful for comparing terms, it would not be unreasonable to conclude the interexperimental differences in algal perfor- that the algae would react and to show signs of mances. ‘photoinhibition’ (see below). Jewson and Wood Kirk (1994)described the several attempts that (1975)showed that continuing to circulate the have been made to find a mathematical expres- algae through the light gradient not only spared sion that gives a reasonable fit to the observed thealgae the symptoms of photinhibition but relationship of P to I. Jassby and Platt (1976) that the measured Pmax could be sustained. In tested several different expressions then available an analogous experiment, Marra (1978)showed against their own data. They found the most suit- that realistically varying the incident radiation able expressions to be one modified from Smith received by phytoplankton avoided the apparent (1936)andtheonethey themselves proposed: photoinhibition. Harris and Piccinin (1977) determined photosynthetic rates (from oxygen pro- = − α − / P Pmax [1 exp( Iz Pmax)] duction, measured with electrodes rather than (Smith, 1936) (3.6) by titration) in bottled suspensions of Oocystis > P = Pmax tanh(α − Iz/Pmax) exposed to high light intensities ( 1300 µmol photons m−2 s−1)and temperatures (>20 ◦C) for (Jassby & Platt, 1976) (3.7) varying lengths of time. Their results suggested In contrast, the significance and mathematical that an elevated photosynthetic rate was main- treatment of the right-hand part of the P vs. tained for 10 minutes or so but then declined Iz curve, corresponding to the apparent near- steeply with prolonged exposure. Either the algae surface depression of photosynthesis in field were photoinhibited or damaged or they had experiments, was, for a long time, a puzzling reacted to prevent such damage (photoprotec- feature. It was not necessarily a feature of all tion) in some way that would enable to retain P vs. z curves: some of the possible variations their vitality to maintain growth (see Section are exemplified inFig.3.4.Anomalies in the 3.3.4). depth distribution of NP, caused by phytoplank- Forthese reasons, determinations of depth- −2 ton abundance (Fig. 3.4a), low water temperature integrated photosynthesis (NP,inmgO2 m (Fig 3.4c) or by surface scumming of dominant h−1)neednolongerneeddependontheplani- Cyanobacteria (Fig. 3.4d) fail to obscure the inci- metric measurement of the area enclosed by the dence of subsurface biomass-specific photosyn- measurements of photosynthetic rates against thetic rates. However, they are not seen when dull depth. They are estimable, for instance, from the skies ensure that, even at the water surface, pho- Pvs.Iz curve in Fig. 3.3f, as the area of a trapez- tosynthetic rates are not light-saturated [z(Ik) < 0 ium equivalent to Pmax × 2[(I0 – Ik) + (I0 − Ic), m!]. where I0 is the light intensity at the water sur- This near-surface depression in measured pho- face and Ic is the intercept of zero photosynthe- tosynthertic rate is not, however, reflected in sis. In terms of P vs. depth, this simplifies to the LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 105

product Pmax × (the depth from the surface to the point in the water column where the light will half-saturate it); i.e.

≈ × NP P max z(0.5Ik) (3.8)

If the dark respiration rate, NR,isuniformwith Figure 3.5 Hypothetical P vs. I plots to contrast seasonal depth, then the integral is simply the product of variations in temperature on photosynthetic behaviour, with the full depth range over which it applies (the special reference to changes in Pmax (tagged) and Ik height of the full water column, H)depth (arrowed). In either plot, the sequence a→b→cisone of increasing temperature. In the left-hand plot, the dependence NR ≈ R × H (3.9) upon light is constant; in the right-hand plot, P/I varies to keep Ik constant. Redrawn from Reynolds (1984a).

Based upon the numerous published records, several compendia of the key indices of photosyn- lated by rearranging Eq. (3.5): thetic oxygen production of phytoplankton in −1 −1 α = Pmax/Ik = 2.28 mgO2 (mg chla) h closed bottles have been assembled (Harris, 1978; / −2 −1 Kirk, 1994;Padisak,´ 2003). Clearly, the gross rate 48µmol photons m s = . −1 −1 of photosynthesis (NPmax) and the depth integral 0 0475 mgO2 (mg chla) h (NP)respond to two variables, which are, within (µmol photons m−2s−1)−1 limits, highly variable. Other factors notwith- −1 −1 2 = 13.2mgO2 (mg chla) (mol photon) m standing, observed Pmax should always be the light-saturated maximum rate at the given tem- Comparisons among differing P vs. I plots perature. Among the fastest reported examples often differentiate patterns of photosynthetic −1 −1 are 30–32 mg O2 (mg chla) h (noted in warm behaviour. In the left-hand box of Fig. 3.5,the tropical lakes in Africa, by Talling, 1965;Talling slopes (α) show similar light dependence of pho- et al., 1973;Ganf, 1975), whereas the specific photosynthesis at low irradiances but the sequence tosynthetic rates in temperate lakes rarely exceed of increasing Pmax values could be the response of −1 −1 the 20mgO2 (mg chla) h found by Bind- thesame alga to increasing temperatures. In the loss (1974). Thus, as might be expected, examples right-hand plot, data for three different algae are of high community rates of oxygen production shown, all saturating at similar levels but with come from warm lakes supporting large popu- differing photosynthetic efficiencies. A higher α lations of phytoplankton algal chlorophyll and enables a faster rate of photosynthesis to be main- when there are also ample reserves of exploitable tained when light intensity is low. −3 −1 CO2:integrals in the range 6–18 g O2 m h have been noted in Lac Tchad, Chad (Lévêque 3.3.2 Measurement of light-dependent et al., 1972), Red Rock Tarn, Australia (Hammer photosynthetic carbon fixation et al., 1973)andLake George, Uganda (Ganf, 1975). On the basis of an equimolecular photosynthetic The onset of light saturation, Ik,isalsotempera- quotient (PQ ∼ 1), the light efficiency of photo- ture influenced but is generally <300 µmol pho- synthesis could be calculated from the oxygen tons m−2 s−1. There are many citations of much evolution data to be ∼5.0 mg C (mg chla)−1 (mol −1 2 lower Ik determinations, 15–50 µmol photons photon) m . This is actually below the average m−2 s−1,generally at temperatures <10 ◦C (Kirk, of a large number of extrapolated values, which 1994). The most consistent values seem likely to fall mainly in the range 6–18 mg C (mg chla)−1 relate to the slope, α,which,atlowlightlevels,is (mol photon)−1 m2 (Harris, 1978). However, for less dependent on temperature and more depen- over 50 years now, it has been possible to work dent upon light-harvesting efficiency. Taking the directly in the currency of carbon, applying the plot in Fig. 3.3f, the slope α (i.e. P on I) is calcu- so-called 14 Cmethod of Steemann Nielsen (1952) 106 PHOTOSYNTHESIS AND CARBON ACQUISITION

Since its introduction, the method has been Ta b l e 3.1 Temperature-sensitive characteristics of light-dependent carbon fixation. For reported data on improved in detail (the liquid-scintillation and gas-phase counting technique is nowadays pre- maximum photosynthetic rates (Pmax) and on the onset of light saturation (Ik), the majority of ferred) but, in essence, the original method observations fall within the ranges shown in the has survived intact (Søndergaard, 2002). Provid- brackets; extreme values are shown outside the ing proper licensing and handling protocols are brackets. Under conditions of light limitation followed meticulously, the method is easy to < (Iz Ik), temperature dependence of photosynthesis is apply and yields reproducible results. Compar- weaker and the single range of photosynthetic isons with simultaneous measurements of oxy- efficiencies applies to the available data genevolution normally give tolerable agreement, ∼ Pmax if allowance is made for a PQ of 1.15 (Kirk, 1994). in mg C (mg chla)−1 h−1 Alarge number of results have been published θ 2–5 ◦C 0.5 (1.0–2.6) 3.0 in the literature and these have been the sub- θ 17–20 ◦C 2.5 (3.3–8.6) 9.7 ject of a series of syntheses (including Harris, θ 27–30 ◦C 7–20 1978, 1986;Fogg and Thake, 1987;Kirk, 1994; Ik Padisak,´ 2003). It is sufficient in the present con- in µmol photon m−2 s−1 text simply to summarise the key characteristics θ 2–5 ◦C 17–30 that have been reported (maximum measured θ 17–20 ◦C20(90–150) 320 chlorophyll-specific rates of light-saturated car- θ 27–30 ◦C60(180–250) 360 bon incorporation and the chlorophyll-specific α photosynthetic efficiencies under sub-saturating − in mg C (mg chla) 1 2 (6–18) 37 light intensities (see Table 3.1). − (mol photon) 1 Two comments are important to make, how- m2 ever. One is the positive linkage of light saturation with temperature, at least within the range Source: Generalised values synthesised from the of the majority of observations – between 5 and literature (Harris, 1978; Reynolds, 1984a, 1990, 25 ◦C. As with many other cellular processes, 1994a;Padisák 2003). activity increases with increasing temperatures, up to maximal levels varying between 25 and 40 ◦C. There is a plain dependence for the photo- for measuring the photosynthetic incorporation synthetic rates to accelerate with higher temper- of carbon dioxide labelled with the radioactive atures and, so, for there to be a higher threshold isotope. Still using darkened and undarkened bot- flux of photons necessary to saturate it. With no tles suspended in the light field, the essential change in the strongly light-limited rates of pho- principle is that the natural carbon source is aug- tosynthesis, α may vary little (i.e. light-limited 14 mented by a dose of radio-labelled NaH CO3 in photosynthesis is not temperature-constrained; solution, which carbon source is exploited and left-hand plot in Fig. 3.5). Thus, Ik increases with taken up and fixed into the photosynthetic algae. temperature, in broadly similar proportion to the At the end of the exposure, the flask contents are increase in Pmax. filtered and the residues are submitted to Geiger As a function of customary temperature, Pmax counting (for a recent methodological guide, see increases non-linearly, roughly doubling with Howarth and Michaels, 2000), and the quantity each 10 ◦Crise in temperature. This multiple, thus assimilated is calculated. It is supposed that formalised as the Q10 factor, is now used infre- 14 Cwillbefixedinphotosynthesis in the same quently as a physiological index: preference is 12 proportion to Cthat is available in the pool at now accorded to the slope of reactivity on the start of the exposure. Then, theArrhenius scale, which expresses absolute temperature (in kelvins) as a reciprocal scale, 12 /12 CO2 uptake CO2 available 1/(temperature in K). As an example, the mea- 14 14 = CO2 uptake/ CO2 available (3.10) sured temperature sensitivity of light-saturated LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 107

ing by Steemann Nielsen himself) and, perplex- ingly, these persist to the present day. The most important concerns the metabolic exchanges and cycling of carbon, in which the labelled carbon participates relatively freely. At first, labelled carbon moves in only one direction, from solution to photosynthate; it is a manifestation of gross photosynthesis. As the experiment proceeds, some of the 14 C-labelled carbohydrate may be assimilated but it may just as easily be used in basal respiration, or it may well be subject to photorespiration or excretion (see Section 3.2.3). This means that, as the incubation proceeds, the method is ostensibly measuring something closer to net photosynthesis. Long incubations may determine only 14 Figure 3.6 Mean saturated chlorophyll-specific net photosynthetic Cincorporation (Steemann photosynthetic and dark respiration rates of cultured Nielsen, 1955;Dring and Jewson, 1979). Compar- Asterionella cells in controlled bench-top exposures. Original ing net 14 Cassimilation with net oxygen pro- data of Reynolds (1984a). duction over 24-h incubations, by which time 14 respired CO2 is being refixed, takes PQ closer to 1.4 (see Marra, 2002). photosynthesis and dark respiration of labora- The switches towards this more balanced tory isolates of Asterionella formosa are shown in state ofexchangeswillbeapproached at dif- Fig. 3.6. The normalised, Arrhenius coefficient is ferent rates, depending upon temperature and −18.88 × 10−3 per reciprocal kelvin. In the more theirradiance to which the incubating mate- familiar, if incorrect, terms, Q10 is 2.18. Almost rial is exposed and on the physiological condi- all quoted values, applying both to named species tion of the alga at the outset. The behaviour has and to phytoplankton in general, fall in the range been expressed through various descriptive equa- 1.8–2.25 (Eppley, 1972;Harris, 1978). Some variations (notably those formulated by Hobson et al., tion is probable, not least because photosynthe- 1976; Dring and Jewson, 1982; Marra et al., 1988; sis is a complex of many individual reactions. Williams and Lefevre, 1996). A probabilistic out- However, its maximum, light-saturated rate is pri- come is that the largest proportion of the gross marily a function of temperature (Morel, 1991), uptake of 14 Cisassimilated into new protein and even though the several descriptive equations fit- biomass in healthy cells when they are simulta- tedtoexperimental data differ mutually (Eppley, neously exposed to sub-saturating light intensi- 1972;Megard, 1972)andhavebeen shown to ties. Conversely, with approaching light satura- be underestimates against the maximum growth tion of the growth-assimilatory demand for photo- rates that have been observed (Brush et al., 2002). synthate (recognising that this may be constrai- Whereas photon capture has a Q10 close to 2 ned by factors other than the supply of photo- (see Section 3.2.1), protein assembly and inter- synthate), then more of the excess is vented nal transport have greater temperature sensitiv- or metabolised in other ways. Thus, the ratio ity (Tamiya et al., 1953;seealsoSection 5.3.2 for of net photosynthetic carbon fixation to gross theinfluence of temperature on growth). The Q10 photosynthetic carbon fixation (Pn : Pg)isinthe of steady, dark respiration rates of healthy phyto- proportion of the fraction of the gross photo- plankters is similarly close to 2. synthate that can be assimilated, i.e. (Pg − R)/Pg The second comment is that all these deduc- (Marra, 2002). Here, R may represent not just tions are subject to uncertainties about the preci- thebasal, autotrophic respiration (Ra) but, in sion of the radiocarbon method. Interpretational addition, all metabolic elimination of excess difficulties were recognised early on (includ- photosynthate (Rh). Even under the optimal 108 PHOTOSYNTHESIS AND CARBON ACQUISITION

conditions envisaged, Ra never disappears but is where photosynthesis is entirely compensated by always finite, being, at least, about 4% of Pmax (or respirational loss. This theme is continued in the maximum sustainable Pg at the same temper- Section 3.3.4. ature), and typically 7–10% (Talling, 1957b, 1971; Reynolds, 1984a). Reynolds’ (1997a)bestpredictor Characterising the photosynthetic impact of of basal respiration in a number of named fresh- theunderwater light intensity water phytoplankters at 20 ◦Cisrelated to the Taking first the condition of phytoplankton at a 0.325 surface-to-volume ratio [Ra20 = 0.079 (s/v) ]. On fixed or relatively stable depth in the water col- theother hand, the sum of physiological losses umn, the light energy available to them will, in in light-saturated and/or nutrient-deficient cells, any case, fluctuate on a diel cycle, in step with including that vented as DOC, can be extremely daytime changes in solar radiation, and also on a high, approaching 100% of the fixation rate: the less predictable basis brought about by changes quotient (Pg − R − Rh)/Pg and the ratio Pn : Pg both in cloud cover and changes in surface reflectance fall toward zero. owing to surface wind action. Besides variance This isaplausiblewayofexplaining diffi- in I0,the instantaneous incident solar flux of culties experienced in accounting for the fate PAR on the water surface, there is variance in of the carbon fixed in photosynthesis (Talling, the irradiance in the flux passing to just beneath 1984;Tilzer,1984;Reynoldset al., 1985)and the air–water interface, I0.Reflectance of incom- the sometimes very large gaps between primary ing light is least (about 5%) at high angles of carbon fixation and net biomass accumulation incidence but the proportion reflected increases (Jassby and Goldman, 1974a;Forsberg, 1985). steeply at lower angles of incidence, especially Thus, beyond gaining a broad perspective on the <30o.Wind-induced surface waves modify the constraints acting on chlorophyll-specific photo- reflectance, both reducing and amplifying pene- synthetic rates, it is necessary also for the physi- tration into the water at the scale of milliseconds. ological ecologist to grasp the manner in which Near sunrise and sunset, waves are important to the environmental conditions mould the deploy- maintaining a flux of light across the water sur- ment of fixed carbon into the population dynam- face (Larkum and Barrett, 1983). ics of phytoplankton. Variability in the light income to a water body is represented in the examples in Fig. 3.7. 3.3.3 Photosynthetic production at Measured daily integrals of the solar insolation sub-saturating light intensities input across the surface of Esthwaite Water, UK In this section, we focus on the adaptive mech- (a temperate-region lake, experiencing a predom- anisms which phytoplankters use to optimise inantly oceanic climate) through a period of just their carbon fixation under irradiance fluxes that over one year are shown in the main plot. Besides markedly undersaturate the capacity of the indi- showing a 100-fold variation between the high- vidual light-harvesting centres. To do this, it is est (56.4 mol photons m−2 d−1)and lowest light necessary to relate the light-harvesting capacity inputs (0.5 mol photons m−2 d−1), the plot reveals to the cell rather than to chlorophyll per se,aswe that part of this owes to the substantial annual invoke the number of centres in existence within fluctuation in the maximum possible insola- the cellandtheirintracellular distribution as tion (based on the solar constant, its latitudinal adaptive variables, as well as the role played by correction, the deduction of non-PAR and with accessory pigments. It is also necessary to adopt allowance for albedo scatter in the atmosphere) amorequantitative appreciation of the diminu- due to the location of the lake (54 oN). Superim- tion of harvestable light as a function of increas- posed upon that are the near chaotic fluctuations ing water depth and the contribution to vertical that are due to day-to-day variations in the extent light attenuation that the plankton makes itself. and thickness of cloud cover and which cut the Finally, water movements entrain and transport light income by anything between 2% or as much phytoplankton through part of this gradient, fre- as 94% of the theoretical maximum (Davis et al., quently mixing them to depths beyond the point 2003). The inset in Fig. 3.7 presents two day-long LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 109

Figure 3.7 Main plot: Measured daily insolation at the surface of Blelham Tarn (August 1999 to October 2000), compared to the theoretical maximum insolation, as calculated from the latitude and assuming a clear, dry atmosphere (redrawn with permission from the data of Davis et al., 2003). The insets show the diel course of solar radiation intensity, measured at the same location on an overcast January day and a cloudless day close to the summer solstice. Based on data presented originally by Talling (1973) and redrawn with permission from Reynolds (1997a).

time courses of insolation, measured at the same or latitude by Talling (1971). Despite coming from ε = − / − quite different data sets collected at quite differ- (ln I0 ln Iz) h(0 z) (3.12) ent times, these two extremes amplify the vari- − ation shown in the main plot ofFig.3.7. The where h(0 z)isthevertical distance from the first corresponds to a rainy, overcast winter day surface to depth z. ε on which the aggregate insolation is below 1 From Fig. 3.3d, (0.5 m to 1.5 m) is solved from − ε = −1 mol photons m−2 d−1;the second is a cloud- (ln I0.5 ln I1.5)as 1.516 m .Wemaynow less near-solstice day when the maximum instan- apply this spectral integral of the attenuating taneous insolation reached over 1.6 mmol pho- light to characterise the daytime changes in the tons m−2 s−1. underwater light field (see Fig. 3.8). The plot in Downwelling radiation is subject to absorp- Fig 3.8ashows the reconstructed time course of tion and scatter beneath the water surface, where theirradiance at the top of the water column it is more or less attenuated steeply and expo- of Crose Mere on 25 February 1971. Beneath it nentially with depth, as shown in Fig. 3.3d. This are marked the values of Ik and 0.5 Ik derived attenuation can usefully be expressed by the coef- in the original experiment (Fig. 3.3). For clarity, ficient of vertical light extinction, ε.Onthebasis the same information is plotted on to Fig. 3.8b, of the spectral integration used to translate the now against a natural logarithmic scale. Assum- P vs. depth to P vs. I,thecoefficient may be esti- ing no change in any component save the incom- mated on the basis of the equation ing radiation through the day, Fig. 3.8crepre- sents the diurnal time track between sunrise and −ε = · z sunset of the depths of Ik and 0.5 Ik.Otherfac- Iz I0 e (3.11) tors being equal (including the coefficient of ver- where e is the natural logarithmic base, and tical extinction of light, ε), the depth at which whence chlorophyll-specific photosynthesis can be satu- ratedincreases to a maximum at around the diur- ε =− / / − ln(Iz I0) h(0 z) nal solar zenith, as a function of the insolation 110 PHOTOSYNTHESIS AND CARBON ACQUISITION

Figure 3.9 Depth-integrated community photosynthetic rates (NP)for selected times through the day (07.00, 09.00, etc.) predicted interpolated values of (I ) and the time track Figure 3.8 (a) Hypothetical plot of the time-course of 0 of the depth of I developed in Fig. 3.8. Redrawn from immediate subsurface irradiance intensity (I )on25February k 0 Reynolds (1984a). 1971 (the date of the measurements presented in Fig. 3.3); (b) the same shown on a semilogarithmic plot. In (a) and (b), the contemporaneous determinations of I and 0.5 I are k k (NP,inmgCm−2 d−1). A. E. Walsby and inserted. In (c), the time courses of the water depths reached colleagues have been particularly successful in by irradiance intensities respectively equivalent to Ik and 0.5 Ik are plotted SR, sunrise; SS, sunset. Redrawn from Reynolds developing this approach (using Microsoft Excel 7 (1984a). software), details of which they make available on the World Wide Web (Walsby, 2001;seealso Bright and Walsby, 2000;Daviset al., 2003). The technique is helpful in establishing the envir- (I0). Outside the Ik perimeter, chlorophyll-specific fixation rates are light-limited, as predicted by onmental requirements and limitations on algal the contemporaneous P vs. I curve. For instance, growth. extrapolation of relevant data from the experiment shown in Figure 3.3 allows us to fit selected The impact of optical properties of water on reconstructions of P vs. z curves applying at vari- the underwater light spectrum ous times of the day (see Fig. 3.9). As Kirk’s manual (1994) and several other of his In reality, matters are more complex than contributions (see, for instance, Kirk, 2003)have that, especially if cloud cover (and, hence, the powerfully emphasised, the attraction and use- insolation, I0), or the extinction coefficient is fulness of a single average vertical attenuation altered during the course of the day. The greatest coefficient (ε)remains an approximation of the depth of Ik need not be maximal in the middle complexities of the underwater dissipation of of the day. Modern in-situ recording and teleme- light energy. First, as already established, light is try of continuous radiation make it possible to not absorbed equally across the visible spectrum, track minute-to-minute variability in the under- even in pure water (see Fig. 3.10). Photons travel- water light conditions. Moreover, it is now rel- ling with wavelengths of about 400–480 nm are atively simple to translate light measurements least likely to be captured by water molecules; to instantaneous photosynthetic rates, from the those with wavelengths closer to 700 nm are 30 P vs. I curve, and to integrate them through times more likely to be absorbed. For this reason, depth (NP,inmgCm−2 h−1)and through time water cannot be regarded as being colourless. LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 111

waters of high clarity, a second source of error is encountered. This relates to another fundamental of attenuation: besides being absorbed and scattered, according to the properties of the water, attenuation is modiﬁed perceptibly by the angular distribution of the light, which becomes increasingly diffuse with increasing depth. Kirk (2003)proposed the use of an irradiance weighting of the wavelength-speciﬁc gradient, by integrating light measurements over the entire water column, so that 0 0 w εav = εz Iz dz Iz dz (3.13) ∞ ∞

w where εav is the weighted average attenuation coefficient and εz and Iz are the attenuation coefficient and residual light values at each depth increment. The use of this integral improves resolution of thesubsaturating light levels in clear waters but thesimpler, less precise attenuation coefficient derived in Eq. (3.12)remains adequate for describing the underwater light field in most lakes and many coastal waters, where there may be more Figure 3.10 The absorption of visible light (375–725 nm) humic material in solution and there may be by pure water. Drawn from data in Kirk (1994). more particulate material in suspension. More- over, greater concentrations of algal chlorophyll The selective absorption in the red leaves oceanic also contribute to the rapid relative attenuation waterofhigh clarity distinctly blue-green in of light with depth. The average attenuation coef- colour. This effect is strongly evident at increas- ficient comprises: ing water depths beneath the surface, where the ε = εw + εp + N εa (3.14) most penetrative wavelengths come increasingly to dominate the diminishing light field. In lakes, εw is the attenuation coefficient due to the there is a tendency towards higher solute con- water. As already indicated, there is no unique centrations, including, significantly, of plant or and meaningful value that applies across the vis- humic derivatives. These absorb wavelengths in ible spectrum. The minimum absorption in pure theblue end of the spectrum, to leave a yellow or water, equivalent to 0.0145 m−1, occurs at a wave- brownish tinge to the water, as the older names length of ∼440 nm. The clearest (least absorbing) (‘Gelbstoff’, ‘gilvin’) might imply. Under these cir- natural waters are in the open ocean (Sargasso, cumstances, the averaged extinction coefficient Gulf Stream off Bahamas), where the coefficients (distinguished here as εav)becomes less steep of vertical attenuation at 440 nm (εw440)ofambi- < −1 with depth and cannot strictly be normalised just ent visible insolation (I0)are 0.01 m (various by logarithmic expression. εav or ε as used gener- sources tabulated in Kirk, 1994). Values quoted ally, calculated as in Eq. (3.12)fromtheslope of forthe open Atlantic, Indian and Pacific Oceans −1 Iz on z, εav really has only a local value, applying range between 0.02 and 0.05 m .Amongthe to relatively restricted depth bands. clearest lakes for which data are to hand, Crater To express attenuation of light of a given Lake, Oregon has an exceptionally low coefficient wavelength or within a narrow waveband over- of incident light attenuation (ε ∼ 0.06 m−1:Tyler, comes part of the difficulty but, especially in in Kirk, 1994). High-altitude lakes in the Andes 112 PHOTOSYNTHESIS AND CARBON ACQUISITION

range return values of 0.12 to 0.2 m−1 (Reynolds, 1987b,andunpublished observations). Elsewhere, the effects of solutes contribute to higher average extinction coefficients, in coastal seas (εw > 0.15 −1 −1 m )andfresh waters generally (εw > 0.2 m ). At the other extreme, coloration due to humic staining can be intense; Kirk (1994)tabulated some representative values from estuaries and coastal seas receiving drainage from extensive peatland catchments (Gulf of Bothnia, Baltic Sea; Clyde, Scotland) of 0.4 to 0.65 m−1,fromsomehumic lakes and reservoirs in Australia (1 to 3.5 m−1) and from peat-bog ponds and streams in Ireland (2 to 20 m−1). εp is the attenuation coefficient due to the solid particulates in suspension in the water. The particles may emanate from eroded soils or resuspended silts or biogenic detritus. Fine precipitates, for instance, of calcium Figure 3.11 The chlorophyll-specific area of light carbonate, also contribute to particulate tur- interception by algal cells as a function of size and shape bidity. The most persistent are clay particles (•, spherical cells; , non-spherical cells). The straight line < (typically 5 µm), eroded from unconsolidated corresponds to a diminishing efficiency of light interception deposits, which, by absorbing and backscatter- by cells of increasing size but very small cells also lose ing the photon flux, can impart high turbid- efficiency at sizes close to the wavelength of light. Redrawn ity. In many lakes and seas, the contribution with permission from Reynolds (1987b). of background turbidity to attenuation may be trivial (<0.05 m−1)butKirk (1994)cites many examples where it is anything but trivial; canals, part, due to the size and shape of the algae (see rivers, meltwater streams flowing into lakes or Fig. 3.11). Among microplankters, larger quasi- reservoirs can impart attenuation coefficients of spherical shapes, having larger volumes, hold 1to4m−1,withextreme values in the range absolutely greater amounts of chlorophyll than 10–20 m−1.Investigating the turbidity of the smaller shapes. Relative to the cross-section pre- tidally mixed estuary of the Severn, UK, Reynolds sented to the light field, however, the chloro- and West (unpublished data, 1988)found a cor- phyll is more compactly arranged in larger units relation between εp and the mass of suspended and more light passes between them than in clay and fine silt, such that an attenuation coef- smaller units carrying the same amount of ficient of 20 m−1 corresponds approximately to 1 chlorophyll. This approximates to the expecta- −3 2 −1 kg suspended clay m , whence εp ∼ 20 m kg . tions of the ‘packet effect’ (or ‘sieve effect’), Nεa is the attenuation due to phytoplankton. first studied by Duysens (1956)inthe context Evolved to be able to intercept light energy, phy- of solutions and suspensions but developed for toplankton can be, in aggregate, the main com- phytoplankton by Kirk (1975a, b, 1976). How- ponent to vertical attenuation. The extent is pro- ever, among the free-living nanoplanktic and portional to the mass of phytoplankton present picoplanktic cells (<100 µm3), the chlorophyll- per unit volume (N,inmgchla m−3); however, specific area of projection is diminished, to as − thechlorophyll-specific attenuation coefficient, low as 0.004 m2 (mg chla) 1. This may have some- εa,varies considerably. Most general accounts thing to do with the size of plastids being sim- attribute attenuation coefficients of between 0.01 ilar to the wavelength of light. Alternatively, it to 0.02 m−1 (mg chla m−3)−1,or,moresimply, might be explained by the second anticipated 0.01 to 0.02 m2 (mg chla)−1.Variations are, in source of variation, the chlorophyll content of LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 113

components may well dominate over the others. In Fig. 3.13,instances of high attenuation due to arelatively high εw (in the humic Mt Bold Reser- voir, Australia), εp (in the P. K. le Roux Reservoir, South Africa) and Nεa (in an Ethiopian soda lake) are compared with the transparency of a mountain lake (2800 m a.s.l.) in the middle Andes. In each of these relatively deep-water examples, the gradient in Iz is exclusively related to the depth and to the coefficient of attenuation. The same principles apply in shallow waters but, because light can reach the bottom and be reflected back into the water column, the gradient of Iz may not be so steep or so smooth as that shown in Fig. 3.13 (discussion in Ackleson, 2003). Neverthe- less, the present examples give a feel for the column depth in which diurnal photosynthesis can Figure 3.12 Carbon-specific area of freshwater planktic be light-saturated (Iz > Ik > (say) 0.1 mmol pho- algae (ka) plotted against the dimensionless shape index, −2 −1 − − tons m s ) and, more to the point, the vertical msv 1. Near-spherical algae line up close to msv 1 = 6, smaller species tending to have greater interception extent of the water column where phytoplank- properties than larger ones. Shape distortions increase msv−1 ters need to adapt their light-harvesting potential without sacrifice of ka. The algae are Ana, Anabaena to be able to match their capabilities for carbon flos-aquae; Aphan, Aphanizomenon flos-aquae; Ast, Asterionella fixation. formosa; Chla, Chlamydomonas; Chlo, Chlorella; Cry, Cryptomonas ovata; Eud, Eudorina unicocca; Fra, Fragilaria crotonensis; Lim red, Limnothrix redekei; Mic, Microcystis aeruginosa; Monod, Monodus; Phytoplankton adaptations to sub-saturating Monor, Monoraphidium contortum; Per, Peridinium cinctum; Pla irradiances ag, Planktothrix agardhii; Plg, Plagioselmis; Sc q, Scenedesmus quadricauda; Tab, Tabellaria flocculosa. Redrawn with Several mechanisms exist for enhancing cell- permission from Reynolds (1997a). specific photosynthetic potential at low levels of irradiance. One of these is simply to increase the cell-specific light-harvesting capacity, by adding thecells, relative to (say) cell carbon. Plotting ka, to thenumber of LHCs in individual cells. This the areaprojectedper mol of cell carbon, against may be manifest at the anatomical level in the an index of shape (msv−1 is the product of the synthesis of more chlorophyll and deploying it in maximum dimension and the surface-to-volume more (or more extensive) plastids placed to inter- ratio), shows the package effect to be upheld for cept more of the available photon flux falling on quasi-spherical units (from Chlorella to Microcystis; the cell. Most phytoplankton are able to adjust msv−1 = [d4π(d/2)2/4/3π(d/2)3] = 6), while distor- their chlorophyll content within a range of ±50% tion from spherical form usually enhances the of average and to do so within the timescale area that the equivalent sphere might projec- of one or two cell generations. For example, tion (Reynolds, 1993a)(seealsoFig.3.12). Note Reynolds (1984a)made reference to measure- that the individual carbon-based projections are ments of the chlorophyll content of Asterionella less liable to variation than the chlorophyll-based formosa cells taken at various stages of the sea- derivations. sonal growth cycle in a natural lake, during The attenuation components self-compound which the cell-specific quota fluctuated between (Eq. 3.14)toinfluencethediminution of the 1.3 and 2.3 mg chla (109 cells)−1,i.e. 1.3–2.3 pg depth to which incident radiation of given wave- chla (cell)−1. Supposing the capacity of the Aster- length penetrates (Eq. 3.11). In some extreme ionella to fix carbon tohavebeenasmeasuredin instances of attenuation with depth, one of the Fig. 3.3,equivalent to ∼0.8 mg C (mg chla)−1 h−1, 114 PHOTOSYNTHESIS AND CARBON ACQUISITION

Figure 3.13 Some examples of light penetration and (inset) components of absorption due to water and solutes (unshaded), non-living particulates (hatched) and phytoplankton (solid). Laguna Negra, Chile (a), is a very clear mountain lake; (b) Mount Bold Reservoir, Australia, is a signiﬁcantly coloured water; (c) P. K. le Roux Reservoir, South Africa is rich in suspened clay; (d) Lake Kilotes, Ethiopia is a shallow, fertile soda lake, supporting dense populations of Spirulina. Various sources; redrawn with permission from Reynolds (1987b).

then the cells with the lower chlorophyll a com- mation for cells exposed to other than very low plement would havefixed1.04mgC(109 cells)−1 light intensities. h−1,or0.012mgC(mg cell C) h−1.Otherthings It appears that, over successive generations, being equal, the cells with the higher chloro- phytoplankton vary the amount of chlorophyll, phyll complement might have been capable of both upwards (in response to poor photon fluxes) fixing 1.84 mg C (109 cells)−1 h−1,or0.022 mg C and downwards (when similar cells of the same (mg cellC)h−1. The main point, however, is that species are exposed to saturating light fluxes). the cells with the higher chlorophyll content are This represents an ability to optimise the alloca- capable of fixing the same amount of carbon as tion of cellular resources in response to the par- those with the lower complement but at a lower ticular internal rate-limiting function, bearing in photon flux density: in this instance, the high- mind that the synthesis and maintenance of the chlorophyll cells achieve 1.04 mg C (109 cells)−1 light-harvesting apparatus carries a significant h−1 not at ≥48 µmol photons m−2 s−1 but at ≥27 energetic cost and no more of it will be sponsored µmol photons m−2 s−1. The extra chlorophyll a than a given steady insolation state may require increases the steepness of biomass-specific P on I (Raven, 1984). Moreover, under persistently low (the slope α). average irradiances, there is plainly a limit to The measurements of biomass-specific chloro- theextra light-harvesting capacity that can be phyll a referred to in Section 1.5.4 range over installed before the returns in cell-specific pho- an order of magnitude, between 0.0015 and ton capture diminish to zero. If all the photons 0.0197 pg µm−3 of live cell volume. This corre- falling on the cell are being intercepted, more sponds approximately to 3 to 39 mg g−1 of dry harvesting centres will not improve the energy weight (0.3 to 3.9%) or, relative to cell carbon, 6.5 income. On the other hand, this logic indicates to 87 mg chla (g C)−1. Many of the lowest val- theadvantage (preadaptation?) of having a rel- ues come from marine phytoplankters in culture atively large carbon-specific area of projection. (Cloern et al., 1995); most of the highest come Most of the species indicated towards the top from cultured or natural material, but grown of Fig. 3.12 are able to operate under relatively under persistent low light intensities (Reynolds, low photon fluxes, in part, through enhance- 1992a, 1997a). The data show that the frequently ment of the chlorophyll deployment across the adopted ratio of cell carbon to chlorophyll con- light field available. Many of the slender or fil- tent (50:1, or 20 mg chla (gC)−1]mustbeapplied amentous diatoms, as well as the solitary fila- with caution, though it remains a good approxi- mentous Cyanobacteria (Limnothrix, Planktothrix), LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 115 which project perhaps 10–30 m2 (mol cell C)−1, of the alga as much as the independence that perform well in this respect. The quasi-spherical was won. colonies of Microcystis show the opposite extreme Reynolds et al. (1983a)described an analogous 2 −1 (ka: 2–3 m (mol cell C) ). chromatic adaptation of a Cyanobacterium, now Another physiological adaptation to persis- ascribed to Planktolyngbya, stratified in the metal- tent light limitation is to increase the comple- imnion of a tropical forest lake (Lagoa Carioca) ment of accessory photosynthetic pigments. In in eastern Brazil. In each of those cases where general, this assists photon capture by widen- measurement has been made, chromatic adapta- ing the wavebands of high absorbance, effec- tion increased the chlorophyll-specific photosyn- tively plugging the gaps in the activity spec- thetic yield and the cell-specific photosynthetic trum of chlorophyll a.Inparticular, the phy- efficiency (α). In the P. agardhii strain studied by cobiliproteins (phycocyanins, phycoerythrins of Post et al. (1985), the efficiency (α)was∼7 times ◦ the Cyanobacteria and Cryptophyta) and the vari- steeper in cultures grown at20 Cona16h:8h ous xanthophylls (of the Chrysophyta, Bacillario- light–dark cycle and a photon flux of 7 µmol pho- − − phyta and Haptophyta; see Table 1.1)increasethe tons m 2 s 1 than in material in similarly treated − light harvesting in the middle parts of the visi- cultures exposed to >60 µmol photons m 2 −1 −1 ble spectrum. The close association of accessory s (0.78 vs. 0.11 mg O2 (mg dry weight) (mol − pigments with the LHCs facilitates the transfer photon) 1 m2;or,intermsofcarbon, approx- − of excitation energy to chlorophyll a. The corol- imately 0.54 vs. 0.08 mol C (mol cell C) 1 (mol − lary of widening the spectral bands of absorption photon) 1 m2). Supposing a basal (dark) rate of ◦ is a colour shift, the chlorophyll green becom- respiration for Planktothrix at 20 C (derived from 0.325 ing masked with blues, browns or purples. This [Ra20 = 0.079 (s/v) ]; see Sections 3.3.2 and 5.4.1) − − − is acknowledged in the term ‘chromatic adap- of 0.064 mol C (mol cell C) 1 d 1,or0.74 × 10 6 − − tation’ (Tandeau de Marsac, 1977). Some of its mol C (molcellC) 1 s 1,itispossible to deduce best-known instances involve Cyanobacteria for- that compensation is literally achievable at ∼1.4 − − merly ascribed to the genus Oscillatoria. Post et al. µmol photons m 2 s 1.Realistically, allowing for (1985)described the photosynthetic performance faster respiration during photosynthesis and for of a two- to three-fold increase in the chlorophyll the dark period (8 h out of 24 h), net photosyn- content and a three- to four-fold increase in c- thetic gain is possible over about 3 to 4 µmol − − phycocyanin pigment in low-light grown cultures photons m 2 s 1. of Planktothrix agardhii.Photosynthetic attributes Even this performance may be consider- of pink-coloured, deep-stratified populations of P. ably improved on by stratified bacterial pho- agardhii were investigated by Utkilen et al. (1985b). tolithotrophs, with net growth being sustained − − Aremarkable case of chromatic adjustment in by as little as 4–10 nmol photons m 2 s 1 (review anon-buoyant population of Tychonema bourrel- of Raven et al., 2000). Chromatic photoadapta- leyi, as it slowly sank through the full light gration also sustains net photoautotrophic produc- dient in the water column of Windermere, is tion in cryptomonad-dominated layers in karstic given inGanfet al. (1991). Chromatic adaptation dolines (solution hollows) at ambient photon flux − − reaches an extreme claret-colour in populations densities of <2 µmol photons m 2 s 1 (Vicente of Planktothrix rubescens, which stratify deep in the and Miracle, 1988). This seems to be accept- metalimnetic light gradient of alpine and glacial able as a reasonable threshold for photoautotro- ribbon lakes (Meffert, 1971;Bright and Walsby, phy in phytoplankton. Deep chlorophyll maxima 2000). The early-twentieth-century appearance of dominated by chromatically adapted cryptomon- Planktothrix at the surface of Murtensee, Switzer- ads have also been observed in somewhat larger land, was popularly supposed to have come from lakes and reservoirs (Moll and Stoermer, 1982), the bodies of the army of the ruling dukes sometimes close to the oxycline, from which of Burgundy, defeated and slain in a battle at short diel migrations, either upwards to higher Murten in the fifteenth century. The connota- light or downwards (to more abundant nutrient tion ‘Burgundy blood alga’ celebrates the colour resources) are possible (Knapp et al., 2003). 116 PHOTOSYNTHESIS AND CARBON ACQUISITION

Photosynthetic limits in lakes and seas valid as a species-specific statement of an indi- It is often convenient to subdivide the water col- vidual plankter’s position in the light gradient umn on the basis of its ability to sustain net relative to its requirement to be able to compen- photosynthesis or otherwise. The foregoing sec- sate its respirational costs. tions demonstrate three functional subdivisions From Eq. (3.12), we can propose: based on the criterion of light availability. In the − h = ln(I /0.5I )ε 1 (3.15) first (the uppermost), light is able to saturate p 0 k photosynthesis (Iz > Ik); in the second, light is a recognising that Ik is a property of the species constraint, being limiting to chlorophyll-specific of phytoplankton present and that its cell-carbon photosynthesis (Iz < Ik), but whose effects may specificity is attributable to its carbon-specific be photoadaptively offset in order to optimise photosynthetic efficiency; i.e. the rateofbiomass-specific photosynthesis. In I = P /α (3.16) the third, evenbiomass-specific photosynthesis is k incapable of compensating the biomass-specific where P is the carbon-specific rate of photosyn- −1 demands of respiration and maintenance (Iz < thesis (in mol C (mol cell C) s ) and α is the effi- −1 −1 2 IP=R). The actual water depths for these irradi- ciency (in mol C (mol cell C) (mol photon) m ). ance thresholds are notionally simple to calcu- This development also infers the value of the late from the I vs. z curve but, of course, they are attenuation coefficient, ε,asabasis for intercom- not fixed in any sense. The immediate subsurface paring aquatic environments. It has the advan- intensity through the solar day and it is subject tage of being a property of the environment to superimposed variability in cloud cover and (albeit a transitory one) although care is nec- atmospheric albedo, as well in the fluctuating essary in citing the waveband being used (ε440, surface reflectance and subsurface scattering by ε530, εav,etc.). Talling (1960, and many later pub- particulates, induced by wind action. Irradiance lications) demonstrated a predictive robustness thresholds translate to given depths only on an in the approximation of euphotic depth from instantaneous basis. the minimum attenuation coefficient as the quo- Despite the self-evident weakness of any tient, 3.7/εmin.Inhis examples, the least attenu- depth–light threshold relationship, it is still valu- ation was in the green wavebands (λ ∼ 530 nm) able to intercompare various underwater light but, as a rough guide to the depth in which pho- environments by reference to the impacts of their tosynthesis is possible in the sea, the relationship light attenuation properties. A commonly cited holds quite well for other wavebands. Table 3.2 is index used in connection with the ability of a included to contrast the photosynthetic limits of water column to support phytoplankton growth the clearest oceans and some of the most turbid is the average depth ‘reached by 1% of surface estuarine waters, on the strength of the approx- irradiance’; this has also been used to define the imation that, for many phytoplankters and for depth of the so-called euphotic zone.Bearing in much of the day-light period, positive net photo- mind that the PAR flux at the surface at mid- synthesis (Pg ≥ Ra)ispossible in the water col- day varies within at least an order of magnitude umn defined by hp = 3.7/εmin.Itisemphasised (200–2000 µmol photons m−2 s−1), the 1% irradi- that almost all the net primary photoautotrophic ance boundary is approximated no more closely production in the sea occurs within the top 100 than 2–20 µmol photons m−2 s−1.Besides the tem- morsoand,inlakes,withinthetop60m.In poral variability in its precise location in the both cases, it is usually much more constrained water column, the quantity also suffers from than this. its conceptual coarseness. Irradiances within this Another, much more convenient measure of range could saturate the requirements of some relative transparency of natural waters is avail- species while simultaneously failing to compen- able, the Secchi disk. Aweighted circular plate, sate the respiration of others. The depth of the painted all-white or with alternate black and euphotic zone (hp)isnotageneralproperty of the white quadrants, is lowered into the water and underwater environment, although it remains the depth beneath the surface that it just LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 117

Ta b l e 3.2 Comparison of the depth of water likely to be capable of supporting net photosynthetic production (hp)insome representative lakes and seas, supposing hp = 3.7/εmin (cf. Talling, 1960). Values of εmin,the minimum coefﬁcient of attenuation across the visible spectrum are taken (1) from Kirk (1994)or(2) from sources quoted in Reynolds (1987b)

−1 Water εmin m hp m Source Oceans Sargasso Sea 0.03 123 (1) Pacific, 100 km off Mexico 0.11 34 (1) Shelf waters 0.15–0.18 20–25 (1) Lakes and reservoirs Crater Lake 0.06 62 (1) Lake Superior 0.10–0.20 18.5–37.0 (1) Windermere (North Basin) 0.28–0.72 5.1–13.2 (2) Crose Mere 0.32–4.20 0.9–11.6 (2) Lake Kilotes 8.20 0.45 (2) Mt Bold Reservoir 1.14 3.25 (2) P. K. le Roux Reservoir 6.39 0.58 (2) Severn Estuary 10–20 0.2–0.4 (2) disappears from view is noted as the Secchi depth It is likely to be wholly beneficial in maintaining or Secchi-disk depth.Itiseasytouse,hasnowork- photosynthetic vigour, just so long as the vertical ing parts to malfunction and, in the hands of extent of entrainment is within the depth range asingleoperater, it can give fairly consistent offering irradiances between I0 to Ik. results. However, these attractions are countered With relatively deeper mixing, however by difficulties of quantitative interpretation of (either as a result of stronger physical forc- its measurements (see Box 3.1). However, docu- ing or of greater underwater light attenuation), mented records of Secchi-disk depth (zs)spana entrained plankters are carried beyond the depth wide range, from 0.2 m to 77 m (Berman et al., of Ik and, in many circumstances, beyond the 1985)andareadequate to separate clear waters productive compensation point. During a period (zs ≥10 m) from the turbid (zs ≤ 3m)andtobe of time (probabilistically, the mixing time, tm: sensitive to temporal changes in the clarity of any see Section 2.6.5), the individual plankter may be one of them. successively exposed to light intensities that are saturating, sub-saturating or altogether inade- Photoadaptation to vertical mixing quate to support net photosynthetic production. This section considers the adaptive responses These effects are represented in Fig. 3.14, where to turbulent entrainment and vertical transport anotional ‘Lagrangian’ path of a single alga, beyond the column compensation point. Vertical moved randomly in the vertical axis by turbulent mixing per se is not necessarily problematic for entrainment through an equally notional light amicroplanktic photoautotroph and, in entrain- gradient (a), is exposed to a predictably fluctuant ing plankters to and from the high solar irradi- photon flux (b). From the prediction of light- ances that may obtain near the top of the water dependent photosynthesis (c), the instantaneous column, may help to avoid the photoinhibition rate of photosynthesis of the phytoplankter is response observed in phytoplankton captured in also now predictable (d). Integrating through static bottles (Jewson and Wood, 1975). Entrain- time, it is clear that the net photosynthetic gain ment resists the development of other restrict- is impaired below the potential of Pmax. More- ing gradients (for instance, of diminishing dis- over, the deeper is the mixed depth (hm) with solved carbon dioxide or accumulating oxygen). respect to the depth of the column in which net 118 PHOTOSYNTHESIS AND CARBON ACQUISITION

Box 3.1 The Secchi disk

Many variants of the Secchi disk have been employed in limnology and plankton science but the recommended standard is made of aluminium and painted white, is 300 mm in diameter and suspended by three cords attached to a single rope about 30 cm above. It is lowered carefully into the water until the observer just loses sight of it. It is often said to measure transparency or light penetration but these are not literally accurate. The image is lost to the observer through scattering of light rays. However, it is a sufﬁciently useful and serviceable instrument for there

to have been several attempts to relate measurements of Secchi-disk depth (zs)to more formal photometric light determinations (Vollenweider, 1974; Preisendorfer, 1976; Stewart, 1976). The quest is not aided by differences between observers or, for a single observer, by differences between sun and cloud or between calm and waves. On the basis of simultaneous measurements, Poole and Atkins (1929)

deduced that zs and ε are in approximate inverse proportion and, thus, that the

product zs × εmin should be roughly constant. Their evaluation of this constant (1.44) is only just representative of the later estimates (1.4 to 3.0, with a mean of

about 2.2: Vollenweider, 1974). Then the light intensity remaining at zs is between

5% and 24% of I0 (mean ∼15%), whence the compensation depth is perhaps 1.2

to 2.7 × zs.

Figure 3.14 (a) Typical depth proﬁle of irradiance absorption; (b) ‘random walk’ of a phytoplankter entrained in the mixed layer of the same proﬁle; (c) simultaneous plot of the photosynthetic rate that can be maintained at given depths (light-saturated above Ik); (d) deduced instantaneous photosyntheyic rate that is maintained by the alga following the trajectory depicted in (b). Redrawn with permission from Reynolds (1997a). LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 119

photosynthesis is possible (hp), the more restric- be shown to be profound. Supposing I0 is 800 tive are the mixing conditions on the prospects µmol m−2 s−1 and ε is 1.0 m−1,then the light of photosynthetic gain. reaching the bottom of an 8-m mixed later would By extension of this argument, the smaller be 0.27 µmol m−2 s−1 and I∗ forthe whole 8-m −2 −1 is hp in relation to hm,then the more difficult layer is just under 15 µmol m s . Doubling the it is to sustain any net photosynthesis at all. It mixed depth to 16 m, means that the light reach- was longatenet of biological oceanography that ing the bottom would be 9 × 10−5 µmol m−2 s−1 the major mechanism permitting phytoplankton and the integral for the 16-m layer would be recruitment through growth depended upon the <0.3 µmol m−2 s−1.Afactor of two in the depth of depth of mechanical mixing relaxing sufficiently mixing changes a light dose expected to sustain relative to light penetration for net photosynthe- significant net photosynthetic gain to one which sis to be sustainable. This relationship was con- will not even satisfy respiration. sidered by Sverdrup et al. (1942), although it is Furthermore, starting on the basis of areal theeventual mathematical formulation of what integrations of measured photosynthesis and resis still known as Sverdrup’s (1953)‘critical depth piration rates versus depth (NP and NR), model’ to which reference is most frequently extrapolations of net photosynthesis over 24 h made. In particular, the idea that the spring may be approximated, as calculated as NP − bloom in temperate waters, in lakes and rivers NR. Forshort enough days (temperate as well as open seas and continental shelves, winters!), high enough attenuation coefficients is dependent upon the onset of thermal strat- and verifiable mixing limits, it is probable ification, at least when it is compounded by a that low or zero rates of observed phytoplank- seasonal increase in the day length, remains a tonincrease are correctly attributed to inade- broadly plausible concept. However, it is lacking quate energy income. To illustrate this, Reynolds in precision, is open to too literal an interpreta- (1997b)reworkedsomeearlier data (Reynolds, tion and is not amenable to simulation in mod- 1978a; Reynolds and Bellinger, 1992)ontheyear- els. The problem is due partly to the perception round observations on the phytoplankton dynam- of stratification (as pointed out previously, lack of ics in the turbid (ε>0.5 m), 30-m deep, eutrophic apronounced temperature or density gradient is Rostherne Mere, UK. He showed that, in the not, by itself, evidence of active vertical mixing). period January–March, net photosynthetic gain Compounding this is the issue of short-term vari- would have been possible only when the mixed ability and the likelihood of incomplete mixing depth was <4mand that the development of within a layer defined by a ‘fossil structure’ (as any significant spring diatom bloom was nor- defined in Section 2.6.4). mally delayed until April. In a classical paper These are important statements regarding an on the whole-column photosynthetic integrals important paradigm, so care is needed to empha- in Windermere, Talling (1957c)showedthat the sise their essence. It is perfectly true, for instance, observed population increase of Asterionella in that mixing to depth does not only homogenise Windermere in the first3to4monthsofthe probable, time-averaged integrals of insolation year would certainly account for a very high pro- but ‘dilutes’ it as well. I used an integral, I∗ portion (around 96%) of the extrapolated inte- (Reynolds, 1987c), to estimate light concentration gral photosynthesis (and, hence, a simultane- in homogeneously mixed layers, based on the dif- ously very low biomass-specific respiration rate) ference between the light availability at the sur- to be able to sustain it. face and at the bottom, as extrapolated from the Later attempts to model the population attenuation coefficient. growth from first principles underestimated the ∗ oft-observed growth performance in Winder- ln I = (ln I + ln I )/2 (3.17) 0 m mere, unless some allowance was made for a where Im is the extrapolated irradiance at the diminishing Monin–Obukhov length (see Section base of the contemporary mixed layer. Solved by 2.6.3)through the spring period (Reynolds, 1990; = · −εzm Eq. (3.11), as Im I0 e ,deepmixing can Neale et al., 1991a). In other words, the actual 120 PHOTOSYNTHESIS AND CARBON ACQUISITION

responses of each of a number (at least 20) of plankters, being simultaneously ‘walked randomly’ through a simulated light gradient, were summated to derive an aggregate for the population. Huisman et al. (1999)used Okubo’s (1980) turbulent-diffusion model and a concept of residual light at the base of the turbulent layer (devised by Huisman and Weissing, 1994)to demonstrate the importance of a critical light threshold and, incidentally, to show up the shortcomings of the literal ‘critical depth’ model. Figure 3.15 Measured daily mean wind speeds at Blelham Though this view has not passed unchallenged, it Tarn, UK, between August 1999 and October 2000 has been supported independently in the theor- (continuous line), and the mixed depth, as calculated from wind speed and temperature of the water column. Redrawn etical consideration of Szeligiwicz (1998). He also with permission from Davis et al. (2003). verifies the point that a critical depth is not the same for all species simultaneously, that those with a lower critical light compensation will per- spring growth, averaged over a number of consec- form better in deeply mixed layers and that their utive years, is really a response to the weakening own adaptive behaviours may modify the critical ‘dilution’ of the incoming light in a diminish- light and critical depth while the environmental ing mixed depth, even though no conventional conditions persist. thermal stratification is yet established. In real- The nature of these adaptive responses to low ity, this is not at all a particularly smooth tem- aggregate light doses in mixed layers is, in many poral progression. The day-to-day variability in ways, similar to those arising from the low aggre- cloud cover and wind forcing continues but the gate light exposure of plankters residing deep in frequency of the sunnier, less windy days does thelight gradient. However, mixed-layer entrain- accelerate, just as the days are lengthening sig- ment offers short bursts (a few minutes) of expos- nificantly. It follows that, as the year advances, ure to relatively high light intensities separated there are more days on which photosynthetic by probabilistically relatively long periods (of the gain, growth and recruitment in the upper water order of 30–40 minutes) in effective darkness. layers is possible. It would seem important for these organisms Another decade of improvements in moni- to undertake as much photosynthesis as pos- toring approaches and in simulation modelling sible in the exposure ‘windows’ to non-limiting techniques permits us to derive a greater resolu- irradiance fluxes, which requires an enhanced tion on the variability in the underwater pho- light-harvesting capacity rather than a wide tosynthetic environment. In Fig. 3.15,the fluc- spectrum of absorption. Phytoplankton reputed tuations in the mixed depth of Blelham Tarn to grow relatively well under deep-mixed condi- (between 0.5 and 12 m) through a winter–spring tions include the diatoms (especially those with period reveal that there is neither a smooth attenuate cells or that form filaments) and cer- nor single abrupt switch between fully mixed tain Cyanobacteria and chlorophyte genera with and stably stratified conditions, more a chang- analogous morphological adaptations (high ing frequency of alternation. The contemporane- msv−1:Reynolds, 1988a); all project substantial ous compensation depth varied between 2 and carbon-specific areas (10–100 m2 per mol cell C) 8m (Davis et al., 2003), net growth being possible but they vary their contents of chlorophyll a when compensation depth exceeds mixing depth. more than accessory pigments. Two other modelling approaches anticipated Mostly these effects have been detected similarly modified views of the Sverdrup criti- through population growth and recruitment in cal depth model. Woods and Onken (1983) con- culture. Turning off the light for a part of the day structed a ‘Lagrangian’ ensemble, in which the soon brings growth limitation into regulation LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 121

Experimentally imposed fluctuations in light- exposure levels on periodicities of days to weeks also affect the composition and diversity of phytoplankton assemblages (Floder¨ et al., 2002). These operate through the replication, recruitment and attrition of successive generations to populations and will be considered in a later chapter (see Sections 5.4.1, 5.4.2). However, to simulate in thelaboratory some of the extreme behaviours observed in the field required observations relating to photoperiods rather shorter than an hour. Robarts and Howard-Williams (1989)described theresponse of a low-light-adapted Anabaena species in a turbid, mixed lake (Rotongaio, New Zealand) whose rate of photosynthesis could Figure 3.16 Growth-rate responses of Cyanobacteria in accommodate exposure to light at the water sur- ◦ ◦ culture at two different temperatures (10 C, 20 C) to face for 6 minutes but was slowed abruptly under various and two photoperiods: (a) continuous light at further exposure. In this instance, the productive −2 −1 27 µmol photons m s and (b) under a6h:18h advantages were to be gained only in the pho- light–dark alternation. (c) shows the daily growth rate in (b) toperiods of less than 6 minutes, to which the extrapolated to 24 h, to show the improved efficiency of organism had clearly adapted. These observations energy use. Data of Foy et al.,(1976), redrawn from Reynolds (1984a). are considered in the context of photoprotection and photoinhibition, in the next section. by light-dependent photosynthesis more than 3.3.4 Photoprotection, photoinhibition light-independent assimilation – exposing algae and photooxidation to saturating light for only 12 or 6 h out of 24 h Against the background of environmental vari- always results in a reduced daily growth rate. ability, there may be superimposed variations in However, photoadaptative responses to shortened the contemporary ambient range of fluctuations, photoperiod raise the rate of biomass-specific subjecting hitherto supposedly acclimated plank- energy harvest to the extent that growth nor- ters to additional demands of accommodation. malised per light hour is raised. This principle Among the most crucial of these is a weakening was memorably demonstrated by Foy et al. (1976) of the mechanical forcing, either as a result of (Fig. 3.16). asharp reduction in the wind speed or of sharp Litchman (2000, 2003) has taken this approach increase in the photon flux (perhaps as the cloud further, exploring the effect of shorter exper- clears) or, as is often the case, the coincidence imental photoperiods and their discrimination of both events. In all these instances, the abrupt among the performances of the test algae. Fluc- shortening of the Monin–Obukhov length is, far tuation periods were varied between 1 and 24 from being the net beneficial influence cited handintensities were varied between 5 and above (in Section 3.3.3), potentially highly dan- 240 µmol photons m−2 s−1.Photoperiod evoked gerous. Part of the hitherto entrained population little photoadaptation at the higher intensities becomes disentrained deep in the water column, but, at lower intensities, differences in species- where the irradiance is markedly sub-saturating. specific responses became evident. In general, Another is retained within a new, much shal- theeffect of fluctuating light tended to be lower, surface circulation, exposed to a much ele- greater when irradiance fluctuated between lev- vated I∗ value and to a probable excess of radia- els alternately limiting and saturating growth tion in the harmful, high-energy ultraviolet wave- requirements. lengths. The greater the previous adaptation to 122 PHOTOSYNTHESIS AND CARBON ACQUISITION

low average insolation and the more enhanced there-reduction of P680 and, hence, the reacti- is their light-harvesting capacity then, clearly, vation of the LHCs. The energy absorbed from the greater is the danger of damage to the cells unused photons continuing to arrive at P680 is re- affected. Analogous risks confront plankters near radiated as fluorescence. This is readily measurable: the surface of lakes becalmed overnight and sub- thespectral signal of emitted fluorescence has ject to rapid post-dawn increases in insolation. In long been used as an index of plankton biomass alesser way, perhaps, even short bursts of strong (an analogue of an analogue: Lorenzen, 1966). light on a mixed layer or lulls in the wind inten- Differences in the spectral make-up of the emis- sity acting on turbid water under bright sun- sion can also be used to separate the organis- shine will result in potentially sharp increases in mic composition of the phytoplankton, at least thephoton flux experienced by individual algae. to the phylum level (Hilton et al., 1989). However, Moreover, this is the fate of isolates of wild pop- because the transfer of electrons from the plas- ulations, sampled from the water column, sub- toquinone pool to PSI is a rate-limiting step, the sampled into glass bottles and then held captive size of the PQ pool is a measure of the photo- at the top of the water column; it is little wonder synthetic electron transport capacity. In this way, that their performance becomes impaired (Harris PSII fluorescence may also be exploited as a sen- and Piccinin, 1977)(see Section 3.3.1). sitive analogue of photosynthetic activity (Kolber In fact, photoautotrophic plankters are and Falkowski, 1993). Light-stimulated in vivo flu- equipped with a battery of defences for coping orescence from cells exposed to a flash of weak with and surviving exposure to excessive solar light in the dark (F0, when all centres are open) radiation levels. As has already been said, some is compared with the fluorescence following a of these have the effect of cutting photosynthetic subsequent saturating flash (Fm, corresponding rate and the response was formerly interpreted to their total closure). The presence of open cen- as ‘photoinhibition’. Strong light certainly can tres quenches the fluorescence signal proportion- inhibit photosynthesis and do a lot of physical ately, so the difference, (Fv = Fm − F0), becomes damage to the photosynthetic apparatus. How- adirect measure of the photosynthetic electron- ever, manyoftheobserved responses are pho- transport capacity available and the extent of toprotective and serve to avoid serious damage thereduction in the quantum yield of pho- occurring to the cell. These are reviewed briefly tosynthesis caused by exposure to high light below; the sequence is more orlesstheonein intensities. which live cells, suddenly confronted by supersat- As a relatively short-term response, the urating photon fluxes, invoke them in response. chlorophyll-a fluorescence yield alters as the Some excellent, detailed reviews of this topic plankters are moved up and down through include Neale (1987), Demmig-Adams and Adams themixed layer. The measurement of fluores- (1992)andLong et al. (1994). cence to investigate the transport and the speed of photoadaptive and photoprotective reactions Fluorescence of phytoplankton to variable underwater light cli- In simply moving upwards from a sub-saturating mates is one of the exciting new areas of applied light to a depth where the photon flux density plankton physiology (Oliver and Whittington, supersaturates not just the demand for growth 1998). but also the carbon-fixing ability of PSI, the entrained cell will experience two almost concur- Avoidance reactions rent effects, evoking two compounding reactions. Provided they are adequately disentrained and The greater bombardment of the LHCs by pho- their intrinsic movements are adequately effec- tons means that some of these now arrive at reactive, motile organisms migrate downwards from tion centres that are still closed, pending reoxi- high irradiance levels. Avoidance reactions have dation of the acceptor quinone, Q A (see Section been observed especially among the larger 3.2.1). At the same time, the accelerated accumu- motile dinoflagellates (see, especially, Heaney lation of PQH2 in the plastoquinone pool slows and Furnass, 1980a; Heaney and Talling, 1980a) LIGHT-DEPENDENT ENVIRONMENTAL SENSITIVITY OF PHOTOSYNTHESIS 123 and larger, buoyancy-regulating Cyanobacteria tion of the xanthophyll cycle in protecting PSII (Reynolds, 1975, 1978b;Reynoldset al., 1987). For from excessive photon flux density operates by non-motile diatoms, a rapid sinking rate may siphoning off a good part of the energy as heat. provide an essential escape from near-surface Many details of the cycle and its fine-tuning ‘stranding’ through disentrainment, especially in are considered by Demmig-Adams and Adams low-latitude lakes. The relatively high sinking (1992). Here, it is important to emphasise how rates in(especially) Aulacoseira granulata may be these adaptations of phytoplankton to high light afactor in the frequency of its role as domi- assist in maintaining photosynthetic productiv- nant diatom in many tropical lakes where there ity. Carotenoids are especially effective in protect- is a diel variation in mixed water depth (see ing cells against short-wave radiation and the risk Reynolds et al., 1986). The effect may be signifi- of photooxidative stress. cantly enhanced by spontaneous acceleration of Compounds specific to the absorption of the sinking rate of cells coping with an abrupt ultraviolet wavelengths, previously known from increase in insolation (Reynolds and Wiseman, thesheaths of epilithic mat-forming Cyanobac- 1982;Nealeet al., 1991b), perhaps as a result of teria of hot springs (Garcia-Pichel and Casten- the withdrawal of the alleged mechanism of vital holz, 1991), where they screen cells from dam- regulation (see Section 2.5.4). aging wavelengths of radiation (max absorption ∼370 nm), have been found recently in the natural phytoplankton of high mountain lakes. Plastid orientation and contraction Laurion et al. (2002)suggested that, together Planktic cells are generally too small for plas- with the carotenoids, these mycosporine-like tid relocation to have the significance it does in amino acids may occur widely among limnetic thecells of higher plants (Long et al., 1994)but, phytoplankton species, especially in response over periods of minutes to hours of exposure to to exposure to ultraviolet wavelengths. Ibel- high light intensities, contraction of the chro- ings et al. (1994) demonstrated just this sort mophores of planktic diatoms lowers the cross- of acclimation of planktic species, especially sectional areas projected by the cell chlorophyll in Microcystis, where the sustained presence (Neale, 1987). of zeaxanthin contributes to an ongoing ability to dissipate excess excitation energy as Protective pigmentation heat. As originally proposed by Paerl et al. In cells exposed to frequent or continuing high (1983), the mechanism substantially protects cells light intensities over a generation time or more, from overexposure of surface blooms to high over-excitation of the PSII LHCs is avoided by light. changes affecting the xanthophylls. These oxy- genated carotenoids are subject to a series of Excretion light-dependent reactions, which, among the In nutrient-limited cells, photosynthate is chlorophytes (as among green higher plants), scarcely consumed in growth. Even under quite results in the accumulation of zeaxanthin under modest light levels, simultaneous accumulation excess light conditions and its reconversion to of fixed carbon and free oxidant in the cell risk violoxanthin on the return of normal light con- serious photooxidative damage to the cell. This is ditions. Among the dinoflagellates and the chrys- countered principally through the production of ophyte orders (sensu lato,hereincluding the antioxidants, such as ascorbate and glutathione. diatoms), an analagous reaction involves the con- High oxygen levels may trigger the Mehler version of diadinoxanthin to diatoxanthin, when reaction in PSI in which oxygen is reduced to light is excessive, with oxidation back to diadi- water (Section 3.2.3). Moreover, high O2 concen- noxanthin in darkness. The reaction is said to be trations (>400 µM) induce the oxidase reaction about 10 times faster than the analogous reac- of RUBISCO, and the photorespiration of RuBP tion in higher plants (Long et al., 1994,quot- to phosphoglycolic acid. Release of glycolate ing the work of M. Olaizola). The principal func- and other photosynthetic intermediates into the 124 PHOTOSYNTHESIS AND CARBON ACQUISITION

waterisone of the ‘healthy’ (cf. Sharp, 1977)ways of photosynthetic production by inorganic car- in which cells of other algal groups regulate bon has been a surprisingly contentious issue. the internal environment by venting unusable Kuentzel (1969) considered the carbon supply to DOC into the medium. This behaviour carries be one of several factors crucial to the develop- important consequences for the structure and ment of algal blooms in response to lake enrich- function of pelagic communities (see Section ment. Shapiro’s (1973)experimental demonstra- 3.5.4). tions of the ability of bloom-forming Cyanobac- teria to grow at high pH levels (indicative of If these fail... deficiencies in the reserves of CO2 in solution) Nevertheless, prolonged exposure of phytoplank- provided very strong support for this view. On ton cells to high light intensities over periods of theother hand, Schindler’s (1971) whole-lake days to weeks usually results in pigment loss, manipulations in the Experimental Lakes Area of loss of enzyme activity, photooxidation of pro- Canada pointed to the direct linkage of produc- teins and, ultimately, death. Such dire conse- tion responses to added phosphorus and nitro- quences to the photosystems and cell structures gen. His data were persuasive. Moreover, the intu- certainly do enter the realm of severe photoinhi- itive supposition of an adjacent, effectively infi- bition and photodamage. Floating scums of buoy- nite reserve of atmospheric carbon dioxide, read- ant Cyanobacteria are especially vulnerable to ily soluble in water, was enough to allay most photodamage; death sequences have been graph- doubts that carbon availability is a significant ically reported by Abeliovich and Shilo (1972). constraint upon the yields of aquatic biomass. In a more recent account, Ibelings and Maberly However, matters did not rest there and much (1998)described the loss of photosynthetic capac- important research has ensued. Crucially, the ity in response to excessive insolation and carbon first point that must be recognised is that these depletion in laboratory simulations of the condi- arguments are not, in fact, directly opposed, tions experienced in surface blooms. nor are they mutually exclusive. The aquatic At lesser extremes, the resilience of cells and sources of inorganic carbon are, indeed, ulti- opportunities for repair may allow recovery of mately plentiful and renewable and do not con- physiological vigour. Thus, the many effects of stitute a biomass-limiting constraint. At the same environmental variability that can lead to a fall time, it has to be accepted that the ambient con- in the net planktic production of photosynthate, centration of dissolved carbon dioxide is highly once universally labelled as ‘photoinhibition’, variable, that it is inextricably linked to the should properly be viewed as a suite of homeo- pH-dependent bicarbonate system and that algal static protective mechanisms. They enable phyto- production is, anyway, a principal driver in the plankton to survive a large part of the full range transformations. The potential role of the carbon of environmental extremes that may be encoun- supply as a rate-limiting constraint on photosyn- tered as a consequence of pelagic embedding (see thetic behaviour is plainly indicated. also the discussion in Long et al., 1994). 3.4.1 Sources and fluxes of available inorganic carbon 3.4 Sensitivity of aquatic The sea-level, air-equilibrated concentration of photosynthesis to carbon carbon dioxide in water at 0 ◦Cis∼23 µM, falling ◦ −1 to ∼13 µMat20C (say, 0.5–1.0 mg CO2 L , sources or ∼0.15–0.3 mg C L−1). Besides being sensitive to temperature, the equilibrium concentration Besides light, a supply of carbon dioxide is depends upon the atmospheric partial pressure essential to normal photosynthetic production. of CO2, which is, in turn, affected by altitude. However, while the necessity of an instanta- In many natural waters, carbonic acid is the neous light source to the fixation of carbon is only free acid present and, thus, the concen- self-evidently axiomatic, the potential limitation trations of alkalinity (base ions), carbon dioxide SENSITIVITY OF AQUATIC PHOTOSYNTHESIS TO CARBON SOURCES 125

theequilibrated mass of gas in solution (again, generally ∼0.3 mg C L−1) complies with Henry’s law and does not exceed the proportionality of thepartial pressure of the gas in contact with the liquid. At face value, the instantaneous carbon capacity of natural waters to support phytoplankton is unlikely to exceed 0.3 mg C L−1 (or about 0.02 mol C m−3). Where present, bicarbonate raises the DIC reserve up to 2 orders of magnitude greater. Supposing a C : Chla of 50, these capacities are equivalent to the supportive capacity for6to600µgchlal−1.Plainly,carbon limitation of the phytoplankton supportive capacity is hardly likely to arise among the many water bodies in the world in which biomass is severely restricted by 1 or 2 orders of magnitude (∼0.6 to 6 µgchla L−1). Neither is the standing biomass of non-calcareous waters prevented from consider- Figure 3.17 The pH–carbon dioxide–carbonate system in −1 natural waters. The relative quantities of the three ably exceeding 6 µgchla L . The instantaneous 2− carbon dioxide availability in even the soft, non- components, CO2, HCO3- and CO3 , determine the pH of the water, as shown in the inset. Changes in the calcareous waters may significantly exceed the concentration of one component shifts the equilibrium. air-equilibrated concentration and some produc- Photosynthetic withdrawal of CO2 can raise pH to the point tion may be maintained when the DIC reserve is 2− where CO3 is precipitated as a calcium salt. For a more exhausted. This inspires queries about the inter- complete explanation, see Stumm and Morgan (1996). nal sources of carbon dioxide and the rates of Redrawn from Reynolds (1984a). their replenishment. The proximal sources of ‘new’ carbon include thesolution of CO2 at the air–water interface, not and pH (acidity) are continuously interrelated. just at the surface of the water body in question In this range, bicarbonate is generally the domi- but in the rainfall leaching the atmosphere and nant anion (0 to ∼3.5 meq L−1;higheralkalinities falling directly or, indirectly, in the overland flow may be associated with alternative solute compo- discharging into it from the surrounding water- sition, sodium or potassium being the dominant shed. The quantities transported to lakes can be cation, rather than calcium). Potentially, bicar- considerable but the concentrations are still sub- bonate may dissociate to release free CO2, accord- ject to equilibrium constraints. That fraction of ing to the reversible reactions shown in Fig. 3.17. theinflow made up from groundwater sources In this way, bicarbonate in solution represents can become relatively enriched with CO2 under an exploitable store of dissolved inorganic carbon pressure (to the extent that some may vaporise −1 (DIC) ofupto42mgCO2 L .Formuchof the when normal air pressure is encountered). Direct time it serves to buffer the water to the mildly vulcanism (through fumaroles) can provide addi- alkaline side of neutrality (pH ∼8.3), potentially tional sources of carbon dioxide to sea water in to the point of calcium carbonate precipitation certain locations. (see Fig. 3.17). In base-poor lakes, this buffering Usually, the major source of DIC is derived capacity is proportionately weaker. In extremely from chemical weathering of carbonate rocks acidic sodium-sulphate waters (pH < 4.5), there and debris in soils, including terrestrially is (by definition) no alkalinity at all and DIC is sequestered atmospheric CO2, which is trans- present only as dissolved carbon dioxide or car- ported in run-off. Anthropogenically increased bonic acid. Here, as in the first case considered, CO2 levels and accelerated erosion have 126 PHOTOSYNTHESIS AND CARBON ACQUISITION

contributed to historic sharp increases in equilibrium, were observed. At such times, the alkalinity in some major catchments, including lake would have been losing CO2 to the atmo- that of the Mississippi River (Raymond and Cole, sphere. In contrast, photosynthetic carbon con- 2003). Significant additional sources of carbon sumption in the summer typically depletes the in lakes may come from deliveries of readily epilimnetic DIC to very low levels (Heaney et al., oxidisable organic carbon, both particulate (POC) 1986), occasionally to zero (pH ∼10.3). At these and in solution (DOC). Anthropogenic sources times, the atmosphere becomes the main photo- (sewage, acid deposition, mine discharge) may synthetic carbon source. be of local importance. Over the year, this lake probably loses three These various carbon sources are available to to four times more CO2 to the atmosphere (up to primary producers and, thence, to assimilation 2.8 mol m−2 a−1)than it absorbs (Maberly, 1996). in aquatic food webs. In lakes, some of this car- No more than 4% of the annual production of bon may be removed as organisms, their wastes biomass was found to be attributable to CO2 solu- or cadavers, either to the sediments, or to down- tion across the water surface. Most of the net stream transport, eventually becoming part of resource influx arrives in the lake in solution in thePOC flux to the sea. What is usually rather the inflow streams. As elsewhere, the main part alargerpart of the biogenically assembled car- of the annual load of free CO2 is roughly propor- bon is respired by the producers or metabolised tional to the hydraulic load and the bicarbonate and respired by their heterotrophic consumers load is, approximately, the product of the mean (grazers and decomposers), mostly back to car- bicarbonate alkalinity in the inflow and the num- bon dioxide. This gas can now be vented to the ber of annual hydraulic replacements. atmosphere by equilibration. In lakes, especially, The idea that smaller lakes and rivers are not and at times of low biological activity, carbon necessarily net sinks for atmospheric CO2 but, dioxide is present in solution at concentrations rather, may often be outgassing CO2 to the atmo- considerably over those predicted by Henry’s law sphere, is relatively new (Cole et al., 1994;Cole (Satake and Saijo, 1974). In deep, oligomictic and and Caraco, 1998). In the wet tropics, catchment meromictic lakes, hydrostatic pressure adds to sources of CO2 can make an especially signifi- thelevel of carbon-dioxide supersaturation that cant contribution to the dissolved content and is possible. Mechanical release of such reserves, to losses back to the atmosphere (Richey et al., such as occurred at Lake Nyos, Cameroon, in 2002). In yet another study, Jones et al. (2001) cal- 1986, carries dire consequences for people and culated that net CO2 efflux from temperate Loch livestock in the adjacent hinterland (see Loffler,¨ Ness may represent around 6% of the net ecosys- 1988). temproduction of the catchment. It becomes clear that there is a wide range Proportionately, the amount of carbon diox- of carbon availabilities among lakes and seas, ide loaded hydraulically must diminish with as there is in the principal carbon sources. The increasing size of the water body, as (presum- stores and supplies can often be adequate but, ably) the proportion of the carbon dioxide influx at times, demand is capable of exhausting them contributed by net inward invasion across the faster than they can be replenished. This can be watersurface increases. Yet it is plain that, even especially true in individual lakes having high in Esthwaite Water, there are times of high biomass-supportive capacities and making strong carbon demand and low resource-renewal rate, seasonal demands on the carbon flux. Maberly marked by high pH values (∼10) when the accel- (1996) constructed a balance sheet of annual car- erated absorption of atmospheric carbon diox- bon dioxide exchanges in Esthwaite Water (Cum- ide across the water surface must supplement bria, UK), a small (1.0 km2), stratifying (15 m), soft- thetruncated terrestrial and internally recycled water (alkalinity: 0.4 meq L−1)buteutrophic lake. sources. During the autumn, winter and spring, free-CO2 In water bodies much larger than Esthwaite concentrations of up to 120 µM(1.4mgCL−1), Water, thehydraulic loads are relatively very almost seven times the expected atmospheric much smaller and the oxidation of external POC SENSITIVITY OF AQUATIC PHOTOSYNTHESIS TO CARBON SOURCES 127 may be equally diminished on a relative scale. pH, but they create the conditions for carbon In this case, the exchange of carbon dioxide is limitation of their own photosynthesis, at least mediated mainly by respiration and the dynam- until the demand falls or other sources of car- ics tend to be dominated by metabolic turnover, bon can assuage it. In the open sea, where, it is the losstosedimentary depletion of particulate alleged, atmospheric dissolution represents the carbon and the supplement of ‘new’, invading major resource of new carbon, frequent strong atmospheric CO2. winds may well fulfil one of the criteria of The direction and rate of gas-exchange flux gaseous invasion. The typical low biomass rep- (FC) across the water surface is governed by the resented by oceanic phytoplankton assemblages relationship rarely raises the pH far above neutrality. Even so, themaximum rates of invasion under the con- F = G ξp (3.18) C C CO2 ditions envisaged here can hardly be expected to where ξ is the solubility coefficient (in mol m−3 supply much more than 100 g C m−2 a−1. −1 atmosphere ), pCO2 is the difference in partial pressure of carbon dioxide between water and 3.4.2 Phytoplankton uptake of air, and GC is the gas exchange coefficient, or carbon dioxide linear migration rate (m s−1). In fact, the mag- Given the relatively high half-saturation con- nitude of actual exchanges is difficult to estab- stants for RUBISCO carboxylation (12–60 µM) (see lish. However, the work of Frankignoulle (1988), Section 3.2.3), photosynthetic carbon fixation is Upstill-Goddard et al. (1990), Watson et al. (1991) plainly vulnerable to rate limitation by the low and Crusius and Wanninkhof (2003), who are aquatic concentrations to which CO2 may be among those who have attempted to determine drawn (<10 µM) (see Section 3.4.1). Even with rel- gas-transfer rates by reference to models or to atively plentiful supplies of carbon dioxide, the themovements of sulphur hexafluoride tracer harvesting mechanisms of aquatic plants need (SF6), provides important verifications. The sea- to be well developed(Raven,1991). In the first sonal variability in pCO2 becomes a crucially pow- place, satisfaction of the principal requirements erful driver in those instances when, as in Esth- of planktic cells embedded in the viscous range waite Water,photosynthetic withdrawal from is subject to Fick’s laws of diffusion. The number theaquatic phase takes the air–water difference of moles of a solute (n)that will diffuse across to its maximum (up to 9 × 10−4 atmosphere, an area (a)inunit time, t,isafunction of the i.e. the fastest consumption stimulates the most gradient in solute concentration, Co,(i.e.dCo/dx) rapid invasion of the lake). However, the trans- and the coefficient of molecular diffusion of the fervelocity is accelerated as a function of wind substance (m): −5 −1 speed and surface roughness, from ∼10 ms , − n = am(dC /dx) t mol m2 s 1 (3.19) at wind velocities beneath the critical value of o 3.5–3.7 m s−1,toanorder of magnitude greater, Reynolds (1997a) used data for the single, spher- at 15 m s−1 (Watson et al., 1991;Crusiusand Wan- ical cell of Chlorella (diameter ≤4 × 10−6 m, −12 2 ninkhof, 2003). Given high values of pCO2,the approximate surface area ≤50.3 × 10 m ) corresponding invasion fluxes are calculated to to illustrate the limits of diffusion depen- be in the order of 3–30 × 10−8 mol m−2 s−1,or dence. Given (i) that, for an average small-sized between 31 and 310 mg C m−2 d−1.Onceagain, solute molecule (such as carbon dioxide), m ∼ using the approximate 50 : 1 conversion, this 10−9 m2 s−1,that (ii) the thickness of the adja- is theoretically sufficient to sponsor a produc- cent water layer from which nutrients may be tive increment of only 0.6 to 6 mg chlorophyll absorbed is equal to the cell radius and (iii) m−2 d−1. the concentration of carbon dioxide molecules −1 These calculations fully amplify the observa- beyond is at air equilibrium (11 µmol CO2 L ,or tion that large crops of algae, especially in lakes 11 × 10−3 mol m−3), then Eq. (3.19)issolvedto of low bicarbonate alkalinity, do not just deplete deliver 275 × 10−18 mol s−1.Now,let us assume −18 3 the store of CO2 available, with a sharprisein the volume of the cell (v)is33.5 × 10 m 128 PHOTOSYNTHESIS AND CARBON ACQUISITION

and contains 0.63 ×10−12 mol carbon (Tables 1.2, through the action of carbonic anhydrase. The 1.3). If we also assume every molecule of car- carbon dioxide thus available to the carboxyla- bon dioxide so encountered is successfully taken tion of RuBP is effectively concentrated by a fac- into the cell, then the requirement to sustain tor of 40. the doubling of biomass without change in the The more intensively studied CCM of the internal carbon concentration is a further 0.63 Cyanobacterium Synechococcus also transports and × 10−12 mol C (cell C)−1. While the concentration accumulates carbon dioxide and bicarbonate gradient is maintained, the diffusion rate calcu- ions, achieving concentration factors in the order lated fromEq.(3.19)iscapable of delivering the of 4000-fold (Badger and Gallacher, 1987). Recent entire carbon requirement to the cell in ∼2300 s work has revealed the mechanism and genetic (i.e. just over 38 minutes). control of each of four separate uptake path- Forproportionately lower concentrations ways in Synechococcus PCC7942 (Omata et al., 2002: of carbon dioxide, Eq. (3.19) delivers smaller Price et al., 2002). Two take up CO2 atarela- amounts per carbon per unit time and the time tively low affinity, one constitutive and the other to accumulate the material for the next dou- inducible, involving thylakoid-based dehydroge- bling is correspondingly extended. A concentra- nase complexes. There is a third, inducible, high- −1 tion of 0.3 µmol CO2 L could not sustain a affinity bicarbonate transporter (known as BCT- doubling in less than 1 day, when growth rate 1) that is activated by a cAMP receptor protein would be considered to be carbon limited. With at times of carbon starvation (a fuller discussion pH already close to 8.3, the (uncatalysed) dissoci- is included in Section 5.2.1). The fourth mecha- + ation of bicarbonate would support a continuing nism is a constitutive Na -dependent bicarbonate supply of carbon dioxide. When that too became transport system that is selectively activated (per- exhausted, pH drifts quickly upwards as carbon- haps by phosphorylation). ate becomes the dominant form of inorganic CCMs represent a remarkable adaptation of carbon. some (but not all) photosynthetic microorgan- Many planktic algae avoid (or at least delay) isms to the onset of carbon limitation of pro- carbon-dioxide limitation and slow bicarbon- duction rates. They are energetically expensive ate dissociation through resort to a carbon- to operate and, not surprisingly, are invoked concentration mechanism, or CCM. Although to assist survival and maintenance only under the kinetic characteristics of the key RUBISCO severe conditions of DIC depletion. The photon enzyme (especially its high half-saturation cost of fixation of CO2 concentrated by the cell as requirement for CO2) cannot be modified, the opposed to the harvest at equilibration is roughly CCM provides the means to maintain its activ- doubled (>16 mol photon per mol C fixed) and ity by concentrating CO2 at the sites of car- the compensation point is raised to around 10 − − boxylation. Since their function was first recog- µmol photons m 2 s 1 (Raven et al., 2000). nised (Badger et al., 1980,Allen and Spence, 1981; Lucas and Berry, 1985), the mechanisms assist- 3.4.3 Species-specific sensitivities to low ing survival of low-CO2 conditions have contin- DIC concentrations ued to be intensively investigated. Progress has The differential ability of aquatic plants to utilise been reported in several helpful reviews (Raven, theinorganic carbon supply in fresh waters has 1991, 1997;Badger et al., 1998; Moroney and been recognised as such for several decades. Chen, 1998). Working with the green flagellate However, the association of particular types of Chlamydomonas reinhardtii, Sultemeyer¨ et al. (1991) phytoplankton with particular types of water showed that the algal CCM involves a series of stretches back almost 100 years, to the days of ATP-mediated cross-membrane transfers – at the the Wests and the Pearsalls (West and West, 1909; cell wall, the plasma membrane and the chloro- Pearsall, 1924, 1932)and to the lake classifica- plast membrane – which transport and concen- tion schemes based on biological metabolism trate bicarbonate ions as well as carbon diox- devised by Thienemann (1918)and Naumann ide. Breakdown of the bicarbonate is accelerated (1919). The importance of inorganic nutrients, SENSITIVITY OF AQUATIC PHOTOSYNTHESIS TO CARBON SOURCES 129 nitrogen and phosphorus in particular, in gov- rich in bicarbonate but usually deficient in nitro- erning aquatic metabolism was quickly and cor- genand, partly as a consequence of precipita- rectly appreciated. As the broad correlations tion as hydroxyapatite (calcium phosphate), phos- detected among indicative types of freshwater phorus. The modest phytoplanktic biomass they phytoplankton and the metabolic state of lakes carry is, however, often dominated by the species became developed, particular species or groups of volvocalean green algae, diatoms, dinoflag- of species became classified as indicators of olig- ellates and bloom-forming species of Anabaena, otrophic or of eutrophic conditions (Rodhe, 1948; Gloeotrichia or other Cyanobacteria, that Rodhe Rawson, 1956). Many chrysophyte, desmid and (1948) had associated with nutrient-enriched sys- certain diatom species were seen to be indicative tems. In describing the sparse phytoplankton of oligotrophic, phosphorus-deficient conditions of Malham Tarn, situated in the carboniferous (e.g. Findenegg, 1943). Rodhe (1948)wentasfar limestone formations of northern England, Lund as suggesting that phosphorus levels >20 µgPL−1 (1961)remarkedthat it was ‘quantitatively typi- may actually have been toxic to chrysophytes. On cal of an oligotrophic lake but qualitatively rep- theother hand, Cyanobacteria, especially those resentative of a eutrophic one’. In contrast, plank- species of Anabaena, Aphanizomenon and Microcys- tic elements most indicative of supposedly olig- tis that became abundant as a consequence of otrophic plankton (including diatoms of the gen- anthropogenic eutrophication, were believed to era Cyclotella and Urosolenia,suchcolonial green express a preference for high-phosphorus condi- algae as Coenochloris, Paulschulzia, Pseudosphaerocys- tions. tis and Oocystis of the O. lacustris group, desmid Many of these differences can now be genera such as Cosmarium, Staurastrum and Stau- explained in terms of the chemistry of carbon rodesmus and chrysophytes that might include rather than of other nutrients. There is no ques- species of Chrysosphaerella, Dinobryon, Mallomonas tion that the levels of biomass of phytoplankton and Uroglena)were conspicuously lacking. that may be sustained in a pelagic system are Moss (1972, 1973a, b, c) conducted an impor- related to the resources available and that the tant series of experimental investigations of the amounts of accessible phosphorus or nitrogen or factors influencing the distributions of algae (in the oceans) iron may well be the biomass- associated with the eutrophication of erstwhile limiting resource (see Chapter 4). Because car- oligotrophic lakes. He found systematic differ- bon is unlikely ever to be a capacity-limiting ences in the dynamic responses of algae to vari- resource and because a large body of litera- able pH and/or variable carbon sources to be ture projects a weight of experimental evidence more striking than those due to variation in for species-specific differentials in the uptake theamounts of nutrient supplied (see especially capabilities and requirements in respect of Moss, 1973a), with clear separation between the (especially) phosphorus and nitrogen, it is under- characteristically eutrophic species that could standable that interpretations of species selec- maintain growth at relatively high pH and low tion in terms of available nutrients should per- concentrations of free carbon dioxide, and the sist (Reynolds, 1998a, 2000a). In fact, the experi- oligotrophic, ‘soft-water’ species, which could mental evidence for interspecific differentiation not. Moss’s (1973c) conclusion that the response among the dynamics of planktic algae on the of natural phytoplankton assemblages to nutri- basis of their differential abilities to exploit the ent enrichment (‘eutrophication’) is not depen- supplies of carbon has been to hand for many dent on the principal variant (more or less nutri- years. Now, detailed biochemical and physiologi- ent) but on the productivity demands on the cal explanations are available to support the criti- totality of resources. cal role of carbon in distinguishing ‘oligotrophic’ Talling’s (1976)more detailed experiments and ‘eutrophic’ assemblages. on the capacity of freshwater phytoplankton An indicative anomaly is the example of cal- to remove dissolved inorganic carbon from the careous (marl) lakes set in karstic, limestone water established a series (Aulacoseira subarctica → upland areas. Their waters are, by definition, Asterionella formosa → Fragilaria crotonensis → 130 PHOTOSYNTHESIS AND CARBON ACQUISITION

Ceratium hirudinella/Microcystis aeruginosa)ofotrophic species have no, or only modest, abilities increasing tolerance of CO2 depletion and an in this direction. The species of Aulacoseira and increasing capability of staging large population Anabaena studied by Talling (1976)areintermedi- maxima under alkaline, CO2-depleted condi- ate on this scale. Talling’s deduction that the CO2 tions. The work of Shapiro (1990) confirmed system in natural waters ‘plays a large part in the apparenthighcarbon affinities of several determining the qualitative composition as well Cyanobacteria, especially of Anabaena and Micro- as the photosynthetic activity of the freshwater cystis, which could maintain slow net growth at phytoplankton’ was prophetic. pH > 10. That the supply of carbon, rather Evidence is accumulating to suggest that the than any other factor, is limiting under such carbon dioxide system may be similarly selective high-pH conditions is supported by the fact that in the sea. Normally, upward pH drift in the sea bubbling with CO2 will restore the growth rate used to be considered unusual. With the excep- of Microcystis (Qiu and Gao, 2002). tion of Emiliana huxleyi,the formation of whose On the other hand, Saxby-Rouen et al. (1998; coccoliths was investigated by Paasche (1964), evi- see also Saxby, 1990; Saxby-Rouen et al., 1996) dence for the ability of marine phytoplankters to showed convincingly that the chrysophyte Synura use bicarbonate was still lacking as recently as petersenii is unable to use bicarbonate at all and themid-1980s (Riebesell and Wolf-Gladrow, 2002). gave strong indications that species of Dinobryon The investigations of Riebesell et al. (1993) con- and Mallomonas probably also lack the capability. firmed that certain species of marine diatom Ball (in Moroney, 2001) has presented evidence (Ditylum brightwellii, Thalassiosira punctigera, Rhi- that a number of chrysophyte species, includ- zosolenia alata) appear to depend exclusively on ing Synura petersenii and Mallomonas caudata,lack the diffusive flux of dissolved CO2.Growthrates any known kind of carbon-concentrating mech- became carbon limited at DIC concentrations anism. Lehman (1976) had already shown that below 10–20 µM (0.012–0.024 mg C L−1;pH> 8.1) high phosphorus concentration was no bar to the and stalled completely at <5 µM. The dependence growth of Dinobryon.Reynolds’ (1986b)manipula- upon diffusive transport and non-catalysed con- tions of phytoplankton composition in the large version of bicarbonate becomes more problem- limnetic enclosures in Blelham Tarn (see Section atic among those larger phytoplankters that have 5.5.1), showed that phosphorus was as stimula- arelatively low ratio of surface area to volume, tory to the growth ofchrysophytes (Dinobryon, forthe flux to the boundary layer and the nat- Mallomonas, Uroglena)astoanyotherkindofphy- ural dissociation of bicarbonate is just too slow toplankter, provided that thepHdidnot exceed to compensate the CO2 deficit at the cell surface 8.5. To emphasise the point: neither phosphate in the wake of a high photosynthetic demand. In nor bicarbonate interferes with the growth of contrast, however, some shelf-water species, such these chrysophytes, so long as they have access as Skeletonema costatum and Thalassiosira weissflogii, to free CO2. show no growth-rate dependence on free-CO2 con- It is now easy to interpret these various find- centrations, even at pH levels (>8.5) requiring use ings in the light of understanding about differ- of bicarbonate and/or some method of carbon ential abilities to exploit the various available concentration (Burkhardt et al., 1999). Whether sources of DIC. Eutrophic phytoplankters, includ- carbon dioxide or bicarbonate predominates as ing colonial volvocaleans, many Cyanobacteria theproximal carbon source for the alga is not and several dinoflagellates, are those that toler- altogether clear. Bicarbonate may be taken up ate the low free-CO2 conditions of naturally high- and converted to carbon dioxide by the action of alkalinity lakes. The species found in soft waters theenzyme carbonic anhydrase, hydroxyl being in which enrichment with nitrogen and phos- excreted to balance the charge, so adding to the phorus stimulates greater demands on the DIC prevalence of bicarbonate. Carbonic-anhydrase reserves may well be selected by their ability to activity is also detectable on the outer surface exploit bicarbonate directly and/or to focus car- of these phytoplankters where the use of bicarbon supplies on the sites of carboxylation. Olig- bonate is accelerated, especially in response to CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 131

reducing concentrations of free CO2 (Nimer et al., to thepoint of abandoning chlorophyll pigmen- 1997;Sultemeyer,¨ 1998). However, even the bene- tation. Among the Chromulinales, the resort to fits that this ability brings are finite, amount- phagotrophy seems very strongly associated with ing, in effect, to an acceleration of the re- ashortage of nutrients; though normally pig- establishment of the carbonate system (Riebe- mented, however, cells resorting to bacterivory sell and Wolf-Gladrow, 2002). Carbonic anhydrase are much paler and show reduced photosyn- activity is said to reach its peak at CO2 concen- thetic capacity above a threshold prey density trations of ∼1 µM, (Elzenga et al., 2000) when (references in Geider and MacIntyre, 2002). On dissociation of bicarbonate is likely to yield not the other hand, some of these species (e.g. more than 10–20% of the carbon flux occurring Ochromonas)are prominent nanoplanktic bacteri- at the air equilibrium in sea water. Carbon limi- vores and fulfil a key stage in the microbial loop tation of photosynthetic assimilation and poten- (see Section 3.5). tial growth rate of marine phytoplankton is cer- An ability of Chlorococcales to take up glu- tainly possible and may occur more frequently in cose and other soluble sugars derivatives has high-production waters than has previously been been inferred or demonstrated on several occa- acknowledged. sions (Algéus, 1950:Berman et al., 1977;Lewi- tus and Kana, 1994). Their habitats, which fre- 3.4.4 Other carbon sources quently include organically rich ponds, provide To be able to fix carbon in photosynthesis is theopportunities for assimilating organic solutes the abiding property separating the majority but the relationship appears not to be obligate. of photoautotrophic organisms (‘plants’) from Though sometimes representing a major step in themajority of phagotrophic heterotrophs (‘ani- the carbon dynamics of ponds, the trait is far mals’). This division is by no means so obvious from being obligate; algal heterotrophy neverthe- among the protists where nominally photosyn- less can play an important role in the pelagic car- thetic algaeshowcapacities to ingest particu- bon cycle of large lakes. late matter and bacteria as a facultative or a quite typical feature of their lifestyles. This kind of mixotrophy is seen among the dinoflagellates 3.5 Capacity, achievement and fate and certain types of chrysophyte (mostly chromu- of primary production at the lines). Alternatively, the bacterium-like ability to absorb selected dissolved organic compounds ecosystem scale across the cell surface (‘osmotrophy’) is possessed among some chlorophyte algae (of the Chlorococ- This section is concerned with the estimation cales) and in certain Euglenophyta, and among of the capacity of phytoplankton-based systems cryptomonads (Lewitus and Kana, 1994). to fix carbon, how much of that capacity is Whereas osmotrophy clearly represents a realised in terms of primary product assembled means of sourcing assimilable carbon, without and how much of that is, in turn, processed the requirement for its prior photosynthetic into the biomass of its consumers, including reduction, mixotrophy is generally regarded as a at higher trophic levels. This is no new chal- facultative ability to supplement nutrients other lenge, the questions having been implicit in the than carbon (chiefly N or P) under conditions of earliest investigations of plankton biology. The nutrient limitation of production (Riemann et al., stimulus to pursue them has varied perceptibly 1995;Liet al., 2000). However, there is a valuable over this period, beginning with the objective energetic subsidy to be derived too, although the of understanding the dynamics of biological sys- exploitative opportunity varies (Geider and Mac- tems thitherto appreciated only as steady states. Intyre, 2002); some marine dinoflagellates are From the 1970s, advances in satellite observa- said to be ‘voraciously heterotrophic’, ingesting tion have greatly enhanced the means of detect- other protists. In some lakes, Gymnodinium helvet- ing planetary behaviour and function, while, icum seems to be predominantly phagotrophic, at the other end of the telescope (as it were), 132 PHOTOSYNTHESIS AND CARBON ACQUISITION

revolutionary changes in understanding how from a small number of short, representative fixed carbon is transferred among ecosystem field measurements (i.e. to extrapolate the values components have greatly enhanced the interpre- NP , NR). With alternative techniques for tation of the sophisticated techniques available proxy estimates of biomass and production rates fortheir remote sensing. In the 1990s, study of (remote variable chlorophyll fluorometry; Kolber the fluxes of materials between atmosphere and and Falkowski (1993)andsee Section 3.3.4), the oceanic systems and the means by which they are usefulness of models to relate instantaneous esti- regulated has acquired a fresh urgency, born of mates to water-column integrals over periods of theneed to understand the nature and potential hours to days is self-evident. of the ocean as a geochemical sink for anthro- Integral solutions for calculating primary pro- pogenically enhanced carbon dioxide levels. duction over 24 h were devised some 50 years These researches help to substantiate the fol- ago. Several, generically similar formulations are lowing account, even though it is approached available, differing in the detail of the manner in through a hierarchical sequence of integrals of which they overcome the difficult diurnal inte- capacity, from those of organelles to metapopula- gration of the light field, especially the diel cycle tions of plankters stretching across oceans. More- of underwater irradiance in reponse to the day over, although the productive potential is shown time variation in I0 and its relationship to Ik. to be vast, plankton biomass remains generally Forinstance, Vollenweider (1965)choseanempir- very dilute and broadly stable, and has remained ical integral to the diel shift in I0,employing ± so despite recent increases in atmospheric CO2 thequotient, [(0.70 0.07) I0 max], where is partial pressures, and it is also argued that thelength of the daylight period from sunrise the current flux of carbon through this rarefied to sunset. Extrapolation of NP,inrespect of catabolic system is probably as rapid as it can be. the measured NPmax (or, rather, an empirically fitted proportion, [(0.75 ± 0.08) NPmax], that com- 3.5.1 Primary production at the local scale pensates for the proportion of the day when I0 Subject only to methodological shortcomings < Ik)invokes the coefficient of underwater light and the free availability of exploitable inorganic extinction (ε). The Vollenweider solution is: carbon, the most useful indicator of the poten- NP = (0.75 ± 0.08)NP max × tial primary production, P (or P , sensu P − R ) g n g a × . ± . / . × /ε (see Section 3.3.2) comes from the areal integra- ln([0 70 0 07]I0max 0 5Ik) 1 tion of the instantaneous measurements of pho- (3.20) − − tosynthetic rate (NP,inmgCfixedm2 h 1) Talling (1957c) had earlier tackled the integration (see Section 3.3.1). The productivity, sensu produc- problem by treating the daily light income as tion per unit biomass,measuredinmgCfixed aderivative of the daytime mean intensity, I0, − − (mg biomass C) 1 h 1,isavaluablecomparator. applying over the whole day (). He expressed = However, for periods relating to the recruitment I0 in units of light divisions (LD), where LD / / of new generations, it is helpful to measure (or to ln(I0 max 0.5Ik) ln2), having the dimensions of extrapolate) carbon uptake over longer periods, time. The daily integral (LDH) is the product of comparable, at least, with the generation time LD and ,approximating to: required for cell replication to occur. This gen- LDH = [ln(I /0.5I )/ln 2] (3.21) erally means designing experimental exposures 0max k of 12 or 24 h. Such designs increase the risk of The completed Talling solution, equivalent to Eq. measurement error (through depletion of unre- (3.20)is: plenished carbon, possible oxygen poisoning and NP =ln 2 × NP × × LDH× 1/ε the increasing recycling of ‘old’ carbon; see Sec- max tion 3.3.2). These problems may be overcome by (3.22) mounting contiguous shorter experiments (see Numerically, the two solutions are similar. the notable example of Stadelmann et al.,1974) Applied to the data shown in Fig. 3.3,forexam- −3 but it is generally desirable to integrate results ple, where N = 47.6 mg chla m , Pmax = 2.28 mg CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 133

−1 −1 = = −2 −1 O2 (mg chla) h , 10.8 h, I0 max 800 and about 0.564 g C m d .Relative to the producer −2 −1 −3 0.5 Ik = 24 µmol photons m s ;andsuppos- population (4.8 m × 47.6 mg chla m )thisrepre- −1 −1 ing ε = 1.33 (εmin) = 1.33 (εw + εp + Nεa), where sents some 2.47 mg C (mg chla) d ,oraround −1 2 −1 −1 (εw + εp) = 0.422 m and εa = 0.0158 m (mg 0.05 mg C (mg cell C) d . chla)−1, NP is solved by Eq. (3.20)tobetween Such estimates of local production are the −2 −1 1531 and 2020 mg O2 m d .FortheTalling basis of determining the production of given solution, the daily mean integral irradiance (406 habitats (Pn), the potential biomass- (B-)specific −2 −1 µmol photons m s )isusedtopredictNP productive yields (Pn/B) and the organic carbon −2 −1 = 2119 mg O2 m d .Forcomparison, interpo- made available to aquatic food webs. The pro- lation of the profiles represented in Fig. 3.9 sum- ductive yield may sometimes seem relatively triv- −2 −1 mates to approximately 2057 mg O2 m d . ial insomeinstances. Marra (2002), reviewing Most of the variations in the other integra- experimental production measurements, showed tive approaches relate to the description of the daily assimilation rates in the subtropical gyre of light field. Steel’s (1972, 1973)models used a pro- the North Pacific in the order of 6 mg C m−3 d−1. portional factor to separate light-saturated and However, this rate was light saturated to a sub-saturated sections of the P vs. I curve. Tak- depth of 70 m. Positive light-limited photosyn- ing advantage of advances in automated serial thetic rates were detected as deep as 120 m. measurements of the underwater light field, A. E. Thus, area-integrated day rates of photosynthesis Walsby and his colleagues have devised a means (∼570 mg C m−2 d−1) could be approximated that of estimating column photosynthesis at each iter- are comparable to those of a eutrophic lake. How- ation and then summating these to gain a direct ever, the concentration of phytoplankton chloro- estimate of NP (Walsby, 2001)(seeSection phyll (∼0.08 mg chla m−3 through much of the 3.3.3). upper water column reaching a ‘maximum’ of −3 We may note, at this point, that all these 0.25 mg chla m near the depth of 0.5 Ik)indi- estimates of gross production (Pg;onadaily cates chlorophyll-specific fixation rates in the basis, the equivalent of NP )needcorrec- order of only 60 mg C (mg chla)−1 d−1. Carbon- tion to yield a useful estimate of potential specific rates of ∼1.2 mgC(mg cell C)−1 d−1 are net production (Pn = Pg − Ra,asdefined in indicated. This is more than enough to sustain a Section 3.3.2). Again, taking the example from doubling of the cell carbon and, in theory, of the Fig. 3.3,wemayapproximate NR as the population of cells in the photic layer. It is curi- product, 24 h × H × NR, where mean H ous, not to say confusing, that eutrophic lakes −1 −1 = 4.8 m, R = 0.101 mg O2 (mg chla) h and are often referred to as being ‘productive’ when N = 47.6 mg chla m−3 to be NR ∼ 554 mg ultraoligotrophic oceans and lakes are described −2 −1 O2 m d . The difference with Pg gives the daily as ‘unproductive’. This may be justified in terms estimate of Pn (strictly, we should distinguish it of biomass supported but, taking (Pn/B)asthe as NP n): index of productivity, then the usage is diametrically opposite to what is actually the case. = − NPn NP NR In areal terms, reports of directly mea- −2 −1 = 2057 − 554 mg O2 m d sured productive yields in lakes generally range − − −2 −1 between ∼50 mg and 2.5 g C m 2 d 1 (review of = 1.503 g O2 m d . (3.23) Jonasson,´ 1978). These would seem to embrace Since many of these approaches were developed, directly measured rates in the sea, according it has become more common, and scarcely less to thetabulations in Raymont (1980). Estimates convenient, to measure, or to estimate by anal- of annual primary production run from some ogy, photosynthetic production in terms of car- 30–90 g C fixed m−2 a−1 (in very oligotrophic, bon. Supposing a photosynthetic quotient close high-latitude lakes and the open oceans that to 1.0 (reasonable in view of the governing condi- support producer biomass in the order of 1–5 tions – see Section 3.2.1), the net carbon fixation mg C m−3 through a depth of 50–100 m; or, in the example considered might well have been say, ≤500 mg C m−2), to some 100–200 g C fixed 134 PHOTOSYNTHESIS AND CARBON ACQUISITION

m−2 a−1 (in more mesotrophic systems and shelf absorption and fluorescence attributable to the waters able to support some 50–500 mg producer phytoplankton (Geider et al., 2001). To do this Cm−3 through depths between 15 and 30 m; i.e. with confidence requires methodological calibra- ∼15 g C m−2), and to 200–500 g C m−2 a−1 among tion and the application of interpolative produc- those relatively eutrophic systems sustaining the tion models (discussed in detail in Behrenfeld fixation of enriched lakes and upwellings, capa- et al., 2002). Most of the latter employ traditional ble of supporting perhaps 1500–5000 mg C m−3 functions (such as those reviewed in the previ- through depths of only 3–10 m i.e. ∼15 gCm−2. ous section); calibration is painstaking and pro- This series is rather imprecise but it serves tracted but the remakable progress in interpret- to illustrate the fact that although the supporting photosynthetic properties of phytoplankton ive capacity of pelagic habitats probably varies has led to synoptic mapping both of the distri- over 3 or 4 orders of magnitude, the annual pro- bution of phytoplankton at the basin mesoscale duction that is achieved varies over rather less and of analogues of the rate of its carbon fixa- than 2 (maximum annual fixation rates of up tion (Behrenfield and Falkowski, 1997; Joint and to 800–900 g C m−2 are possible in some shallow Groom, 2000; Behrenfield et al., 2002). lakes and estuaries). This is mainly because the The beauty, the global generality and the exploitation of high supportive capacity results simultaneous detail of such imagery are awe- in a diminished euphotic depth. There is thus an some. However, its scientific application has been asymptotic area-specific maximum capacity and, first to confirm and to consolidate the previous on many occasions, a diminishing productivity, generalised findings of biological oceanographers sensu production rate over biomass (see also Mar- (e.g., Ryther, 1956;Raymont, 1980;Platt and galef, 1997). Sathyendranath, 1988;Kyewalyanga et al., 1992; see also Barber and Hilting, 2002,forreview). In essence, the main oceans (Pacific, Atlantic, 3.5.2 Primary production at the Indian) are deserts in terms of producer biomass global scale (<50 mg chla m−2) while net primary produc- The rapid advances in, on the one hand, air- tion is assessed to be generally <200 g C fixed borne and, especially, satellite-based remote- m−2 a−1.Inthe high latitudes, towards either sensing techniques and, on the other, the tech- pole, biomass and production tend to be more niques and resolution for analysing the signals seasonal, with maximum production in the six thus detected, have verified and greatly ampli- summer months and least in winter. The great- fied our appreciation of the scale of global net est annual aggregates (200–500 g C fixed m−2 a−1) primary production (NPP). In barely 20 years, the are detected mainly on the continental shelves. capability has moved from qualitative observa- Production ‘hotspots’ (500–800 g C fixed m−2 a−1) tion, to remote quantification of biomass from are located in particularly shallow areas (e.g., the air (Hoge and Swift, 1983;Dekkeret al., 1995) theBaltic Sea, the Sea of Okhotsk), in shelf and on to the detection of analogues of the rate waters receiving nutrient-rich river outfalls (the of its assembly and dissembly (Behrenfeld et al., Yellow Sea, the Gulf of St Lawrence) and in the 2002). The newest satellite techniques can pro- upwellings of major cold currents (e.g., the Peru, vide the means to gather this information in a around Galapagos;´ and the Benguela, Gulf of single overpass. For terrestrial systems, NPP is Guinea). gauged from the light absorption by the plant Satellite remote sensing has also helped to canopy (APAR, absorbed photosynthetically active improve the resolution of global NPP aggregates radiation) and an average efficiency of its util- and their relative contribution to the global car- isation (Field et al., 1998). For aquatic systems, bon cycle. The estimates of total oceanic NPP, sensors are needed to derive the rate of under- based onimagery,convergeonvalues of around waterlight attenuation (from which the magni- 45–50 Pg C a−1.Itisinteresting that previous esti- tude of the photosynthetically active flux den- mates, all based on summations and extrapola- sity at depth is estimable) and the rates of light tions of various in-situ measurements, are mostly CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 135

Ta b l e 3.3 Annual net primary production (NPP) of various parts of the sea and of other major units of the biosphere

Energy invested NPP (Pg C) (J × 10−18) Marine domains Tropical/subtropical trades 13.0 509 Temperate westerlies 16.3 638 Polar 6.4 250 Coastal shelf 10.7 419 Salt marshes, estuarine 1.2 47 Coral reef 0.7 27 Total 48.3 1890 Terrestrial domains Tropical rainforests 17.8 697 Evergreen needleleaf forest 3.1 121 Deciduous broadleaf forest 1.5 58 Deciduous needleleaf forest 1.4 54 Mixed broad- and needleleaf forest 3.1 121 Savannah 16.8 658 Perennial grassland 2.4 94 Broadleaf scrub 1.0 39 Tundra 0.8 31 Desert 0.5 19 Cultivation 8.0 313 Total 56.4 2205

Source: Based on Geider et al. (2001), using data of Longhurst et al. (1995) and Field et al. (1998). within about 50% of this (20–60 Pg C a−1:see per million by volume, or 0.2 g C m−3). Signiﬁ- Barber and Hilting, 2002). Only Riley’s (1944)esti- cant natural abiotic exchanges of carbon with mate of 126 PgCa−1,basedon oxygen exchanges, the atmosphere include the removal due to car- now seems exaggerated. bonate solution and silcate weathering (∼0.3 Pg It is interesting to compare the estimates for Ca−1)but this is probably balanced by releases various parts of the ocean and with other major of CO2 through calcite precipitation, carbon- biospheric units (see Table 3.3). Shelf waters con- ate metamorphism and vulcanism (Falkowski, tribute nearly a quarter of the total oceanic 2002). As is well known, however, ambient atmo- exchanges despite occupying less than about 1/20 spheric carbon dioxide concentration is currently of the area of the seas. Nevertheless, marine pho- increasing. This is generally attributed to the tosynthesis is responsible for just under half the combustion of fossil fuels (presently around 5.5 ± global NPP of about 110 Pg (or 1.1 ×1017 g) C a−1. 0.5 Pg C a−1 and rising) but the oxidation of ter- Much of this carbon is recycled in respiration restrial organic carbon as a consequence of land and metabolism and reused within the year (see drainage and deforestation also makes signiﬁcant also Section 8.2.1). Net replenishment of atmo- contributions (some 1.6 ± 1.0 PgCa−1: data from spheric carbon dioxide would contribute a steady- Sarmiento and Wofsy, 1999,asquotedbyBehren- state concentration (currently around 370 parts feld et al., 2002). In spite of this anthropogenic 136 PHOTOSYNTHESIS AND CARBON ACQUISITION

annual addition to the atmosphere of ∼7PgC, tion by cloud and backscattering by dust, it is the present annual increment is said to be ‘only’ unrealistic to expect much more than 30% of 3.3 (±0.2) Pg C a−1;say∼0.6% a−1 relative to an this to be available to photosynthetic organisms atmospheric pool of ∼500 Pg). The ‘deficit’ (∼3.8 (say 3.6 GJ m−2 PAR). Using the relationships con- PgCa−1)isexplained,inpart, by a verified dis- sidered in Section 3.2.3,thepotential maximum −2 solution of atmospheric CO2 into the sea and, in yield of fixed carbon is 3.6 GJ m /470 kJ (mol C part, by transfers of organic and biotic compo- fixed)−1,i.e. in the order of 7 kmol m−2 a−1,or nents of unverified scale. about 85 kg C m−2 a−1.Thisisabout 100 times Considering that it seems more painful (in the greater than measured or inferred optima. Even short term) to cut anthropogenic carbon emis- if we start with something a little less optimistic, sions, there is currently a great deal of interest such as the PAR radiation measured at the tem- in augmenting net annual flux of carbon to the perate latitude of the North Sea (annual PAR oceanic store of dissolved carbon of around 40 × flux ∼1.7 GJm−2), we still find that no more than 1018 gC (Margalef, 1997). about 1.5% of the energy available is trapped into the carbon harvest of primary production. 3.5.3 Capacity Looking at the issue in the opposite direction, The achievement of even 48.3 Pg across some 360 the minimum energy investment in the carbon × 106 km2 of ocean (note, areal average ∼133gC that is harvested (Table 3.3)byplanktic primary fixed m−2 a−1)should be viewed against the typ- producers is usually a small proportion of that ically small active photosynthetic standing-crop which is available. To produce 50–800 g C m−2 a−1 biomass (on average, perhaps just 1–2 g C m−2, requires the capture of a minimum of 9–144 mol −2 −1 −2 −1 Pn/B ∼ 100). The supportive potential of this photons m a ,equivalent to 2–32 MJ m a , conversion is certainly impressive but it repre- or less than 2% of the available light energy. sents poor productive yield against the potential There are many reasons for this apparent inef- yield were every photon of the solar flux cap- ficiency. The first consideration is the areal den- tured and its energy successfully transferred to sity of the LHCs needed to intercept every photon. carbon reduction. It is possible that the rate is This can be approximated from the area of the constrained; or that the rate is rapid but the individual centre, the (temperature-dependent) producer biomass is constrained; or, again, that length of time that the centres are closed follow- other processes impinge and the productive yield ing the preceding photon capture and, of course, is constrained. thephoton flux density. It was argued, in Sec- These are problems of capacity – how rapidly tion 3.2.1,thattheareaofaPSII LHC (σ X)cov- can production proceed before the metabolic ers about 10 nm2. Thus, in theory, it requires losses might balance the productive gains or aminimum of 1017 LHCs to cover 1 m2.Itwas before the assembly of biomass might become, also shown that 1 g chlorophyll could support subject only to the supply of the material com- between 2.2 and 3.4 ×1018 LHCs and, so, might ponents. The problem will not be addressed fully project anareaof∼22 m2 and harvest photons before the physiology of resource gathering and over its entire area. At very low flux densities, the growth have been addressed (Chapters 4 and 5). intact LHC network (0.045 g chla m−2) has some For the present, we will examine the constraints prospect – again, in theory – of intercepting all of insolation and carbon flux on the biomass of the bombarding photons but, as the flux density phtoplankton that may be present. is increased, it is increasingly likely that photons Commencing with the productive capacity will fall on closed centres and be lost. Saturation of the solar quantum flux to the top of the of the network (Ik)is,infact predicted by: atmosphere (see Fig. 2.2), the income of 25–45 − − − I = (σ t ) 1 photons m 2 s 1 (3.24) MJ m−2 d−1 provides the basis for a theoretical k X c −2 annual income of 12–13 GJ m annually. Tak- where tc is the limiting reaction time (in s −1 ◦ −3 ing only the PAR (46%) and subjecting the flux photon ). At 20 C, when tc ∼ 4 ×10 s(see Sec- to absorption in the air by water vapour, reflection 3.2.1), Ik is solved from Eq. (3.24)as(10× CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 137

10−18 m2 × 4 × 10−3 sphoton−1)−1,i.e.about 2.5 × 10−19 photons m−2 s−1,or∼42 µmol photon m−2 s−1. With supersaturation, more of the photons pass the network or bounce back. Increasing the areal density of LHCs increases the proportion of the total flux intercepted but, in the opposite way, the increasing overlap of LHC projection means that individual LHCs are activated less frequently. There is no light constraint on the upper limit of light-intercepting biomass surface per se, but the cost of maintaining underemployed photosynthetic apparatus and associated organelles is significant. Ultimately, the productive capacity is set not by the maximum rate of photosynthesis but by the excess over respiration. Reynolds (1997b)developedasimplemodel of the capacity of the maximum photon flux to support thefreshwater unicellular chlorophyte Chlorella. Figure 3.18 Comparison of the light-harvesting potential of phytoplankton as a function of biomass, compared with the The alga was chosen for its well-characterised energetic costs of respiration and maintenance. The growth and photosynthetic properties. The ‘max- maximum supportable biomass is that which continues to fix −2 −1 imum’ set was 12.6 MJ m d ,basedupon the just enough carbon in photosynthesis to offset its flux at the summer solstice at a latitude of 52 maintenance requirements. Redrawn with permission from ◦ Nand supposing a dry, cloudless atmosphere Reynolds (2002b). throughout (equivalent daily photon flux, 57.6 mol). Higher daily incomes occur in lower latitudes but the small shortfall in the adopted value an areal concentration of 1/(20.7 m2 (mol cell − − need not concern us here). C) 1) = 0.0483 mol cell C m 2 (or ∼0.58 g C, or − The available light energy is represented by about 11 mg chla m 2). Above this threshold, the vertical axis in Fig. 3.18. The temperature is thecell-specific carbon yield decreases while the assumed to be invariableat20◦C.Arelatively cell-specific maintenance remains constant. Thus, small numbers of cells of Chlorella (diameter 4 forincreasingly large populations, total main- µm, cross-sectional area 12.6 µm2, carbon con- tenance costs increase absolutely and directly tent 7.3 pgCor0.61× 10−12 molCcell−1, carbon with crop size; total C fixation also increases but specific projection 20.7 m2 (mol cell C)−1)arenow with exponentially decreasing efficiency. While introduced into the light field. They begin to har- the daily photon flux to the lake surface remains vestasmall fraction of the flux of photons. At unaltered, the asymptote is the standing crop − − low concentrations, the cells have no difficulty which dissipates the entire 12.6 MJ m 2 d 1 within intercepting the light. At higher concentra- out any increase in standing biomass (somewhere tions, cells near the surface will partly shade out to the right in Fig. 3.18). those beneath them. Even if the whole popula- Taking the basal respiration rate of Chlorella ◦ − − tion is gently mixed, the probability is that cells at 20 Ctobe∼1.1 × 10 6 mol C (mol cell C) 1 − will experience increasingly suboptimal illumi- s 1 (Reynolds, 1990), the energy that would be nation and approach a condition where a larger consumed in the maintenance of the biomass aggregate portion of each day is passed by each present is supposed to be not to be less than − − cell in effective darkness. The onset of subopti- 0.095 mol C (mol cell C) 1 d 1.Tocalculate the mal absorption begins when there is a proba- maximum biomass sustainable on a photon flux − − bilistic occlusion by the Chlorella canopy, i.e. at of 57.6 mol photon m 2 d 1, allowance must be 138 PHOTOSYNTHESIS AND CARBON ACQUISITION

made for the quantum requirement of at least 8 retical phytoplankton concentration that would mol photons to yield 1 mol C and for the frac- generate these light conditions is demonstrably tion of the visible light of wavelengths appropri- equivalent to 650 mg chla m−3 and that it would ate to chlorophyll excitation (∼0.137: Reynolds, absorb some 97% of the incoming light. However, 1990, 1997b). Then the daily photon flux required if the mixing extends to 10 m, Nεa = 4.7, the to replace the daily maintenance loss is equiva- chlorophyll a (470 mg m−2) can now have a max- lent to 0.095 × 8/0.137 = 5.55 mol photons (mol imum mean concentration of only 47 mg m−3, cell C)−1 d−1.Thisistheslope of the straight line accounting for 70% of the light absorbed. If mix- inserted in Fig. 3.18.Itfollowsthat the maximum ing extends 30 m, Nεa = 0.7 and the chlorophyll sustainable population is that which can har- a capacity (70 mg m−2) can have a concentration vest just enough energy to compensate its respi- of no more than 2.3 mg chla m−3, which absorbs ration losses under the proposed conditions, i.e. no more than 10% of the incoming light. 57.6/5.55 = 10.4 mol cellCm−2 (∼125gCm−2). Finally, capacity may also be approximated Notsurprisingly, there is little evidence that from the integral equations for primary produc- quite suchhighlevelsoflivebiomassare tion and respiration. Taking the Vollenweider Eq. achieved, much less maintained, in aquatic envi- (3.20)forNP ,forinstance, capacity is deemed ronments, although it is not unrepresentative to be filled when it is precisely compensated of tropical rainforest. There the true producer by respiration, i.e. when NP = NR,and biomass of up to 100 g C m−2 is massively aug- NP/NR = 1. Giventhat NR is equiv- mented by 10–20 kg C m−2 of biogenic necromass alent to the product, 24 h × H × NR,wemay (wood, sclerenchyma, etc.: Margalef, 1997). In approximate that: enriched shallow lakes, phytoplankton biomass is [0.75 NP × × ln (0.70 I /0.5I ) frequently found to attain areal concentrations max 0max k equivalent to 600–700 mg chla m−2 (Reynolds, ×1/ε]/[24 h × H × NR] = 1 1986b, 2001a), more rarely 800–1000 mg chla m−2 Whence, supposing ε = (εw + εp) + N εa, (Talling et al., 1973;i.e., 30–50 g C m−2). This relative poverty is due, in part, to the markedly N = (1/εa)[0.75 (Pmax/R) × (/24) sub-ideal and fluctuating energy incomes that × . / . ln(0 70I0max 0 5Ik) waterbodies actualy experience. Moreover, fre- × (1/H ) − (ε + ε )] (3.25) quent, weather-driven extensions of the mixed w p layer determine a lower carrying capacity for the The general utility of this equation is realised in entrained population (Section 3.3.3). two ways. First, it can be used to gauge the annual Light absorption by water is a powerful detrac- variation in photosynthetic carrying capacity of tion from the potential areal carrying capacity awater body of known intrinsic light-absorbing that increases with the depth of entrainment. properties (εw + εp)and known seasonal varia- If we solve Eq. (3.17), for instance, against nom- tion in mixed-layer depth (hm in substitution of = = inated values for I0 1000 and for Im 1.225 H). In the application and spreadsheet solution −2 −1 µmol photons m s ,themixed-layer integral of Reynolds and Maberly (2002), (Pmax/R)wasset ∗ −2 −1 2 −1 is I = 35 µmol photons m s , which is suf- at 15 and εa at 0.01 m (mg chla) . ficient to impose a significant energy constraint Second, the equation has been used by on further increase in biomass. From Eq. (3.11), Reynolds (1997a, 1998a)toillustrate the impact of we can work out that the coefficient of attenua- the depth of convective mixing on phytoplankton tion equivalent to diminish 1000 down to 1.225 carrying capacity (reproduced here as Fig. 3.19). −2 −1 µmol photons m s is equivalent to εz = –6.7. Against axes of mixed depth (hm)andbackground Now, supposing that this extinction occurs in a light extinction (εw + εp,withaminimum set, mixed layer extending through just the top metre arbitrarily, for fresh waters at 0.2 m−1)andsup- (z = 1), we may deduce from Eq. (3.14)that ε = posing = 12 h, Fig. 3.19 shows graphically −1 6.7 m = (εw + εp) + Nεa.Putting (εw + εp) = how the maximum chlorophyll-carrying capacity −1 2 −1 −3 0.2 m and εa = 0.01 m (mg chla) ,thetheo- is diluted by mixing, from ∼150 mg chla m in CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 139

low (Talling, 1966;Pollingher and Berman, 1977; Peterson, 1978;Heckyand Fee, 1981). Zero net gains in biomass relative to photosynthesis (i.e. carbon fixation is balanced or exceeded by net losses: Reynolds et al., 1985)are observable when plankter growth isresistedbythetotal exhaustion of one or other of the essential nutrients. The relatively stable biomass of low- latitude oceanic phytoplankton, in spite of positive carbon-fixation rates (Karl et al., 2002), con- formstothe latter diagnosis. The general pattern is that the coupling of net growth to photosynthesis is closest in well mixed, light-limited and nutrient-replete (but possibly carbon-deficient) water columns and weakest under conditions characterised either by stratification, or light saturation to a substantial depth, or extreme nutri- −1 Figure 3.19 Chlorophyll-carrying capacity (as µg chla L ) ent limitations, or any combination of these. of water columns as a function of the depth to which they are That there should be a gap between the mixed (hm) and the background coefficient of light extinction amounts of carbon fixed and those eventually due to colour and suspended tripton (εw + εp). Solutions assume that Pmax/R = 15 and day length is 12 h. Redrawn constituting new biomass is not in itself sur- with permission from Reynolds (1997a). prising, neither is the relative magnitude of the difference. It was once supposed that the shortfall was explicable in terms of mortalities of producer biomass, chiefly to settlement and to consumers and pathogens (Jassby and Gold- a10-mlayerto∼20 mg chla m−3 in a 40-mmixed man, 1974a). Estimating loss rate of biomass was layer and to <1mgchla m−3 in a layer mixed not then well-advanced but the magnitude of to 80 m. Steel and Duncan (1999)developed a biomass losses necessary to explain productive similar model to emphasise the advantages of shortfalls of this order is, on purely intuitive destratifying the eutrophic Thames Valley Reser- grounds, unrealistically large. It was another per- voirs supplying London in order to lower their ceptive analysis (Forsberg, 1985)that pointed out plankton carrying capacity below that of the that, in study after study, the alleged loss of nutrients. biomass was so close to the measured photosynthetic gain that perhaps the ‘lost biomass’ had 3.5.4 Photosynthetic yield to the planktic never been formed in the first place. Instead, the food web losses of fixed carbon are predominantly phys- The purpose of this section is to comment on iological (for instance, through enhanced respi- some aspects of the fate of photosynthetic prod- ration), as had indeed been suggested by both ucts at the local and global level. The profound Talling (1984) and Tilzer (1984). impact that they exert on carbon cycling in The fate and allocation of what, to the pho- plankton-based aquatic systems is also addressed. tosynthetic microorganism, is excess, unassimil- The preceding sections show a wide variation in able and mainly unstorable photosynthate, has theeventual allocation of the carbon fixed in taken a little longer to diagnose. Certainly, a photosynthesis. Well corroborated in the liter- proportion is respired directly, or is fully pho- ature, the range extends from some 92% to torespired to carbon dioxide and water. It had 95% investment in new biomass (Talling, 1957c; already been clear for over a decade, however, de Amezaga et al., 1973;Knoechel and Kalff, that a proportion is excreted as DOC, espe- 1978;GeiderandOsborne, 1992)todisparately cially when cells are stressed by high insolation 140 PHOTOSYNTHESIS AND CARBON ACQUISITION

or depleted nutrititive resource fluxes (Fogg, referred to as the ‘microbial food web’ (Sherr and 1971; Sharp, 1977). The circumstances of gly- Sherr, 1988)or, perhaps, as the ‘oligotrophic food colate excretion, in particular, had been diag- web’. Its short-cutting by direct herbivory is then nosed (Fogg, 1977), well before the circumstances to be seen to be the luxurious exception, possible of its regulated production through the acceler- only when a threshold of relative abundance of ated oxygenase activity of the RUBISCO enzyme nutrient resources is surpassed, sufficient to sus- (see Section 3.2.3)anditsbeneficial role in pro- tain a ‘eutrophic food web’ (Reynolds, 2001a)(see tecting against photooxidative stress had been also Section 8.2.4). elucidated (Geider and MacIntyre, 2002). Many For the present discussion, it is the mecha- other organic compounds are now known to be nisms and pathways of phototrophically gener- released by algae into the water, often in solu- ated carbon that are of first interest. Progress has tion but not necessarily all to do with metabolic been hampered somewhat by an insufficiency of homeostasis. They include monosaccharides, car- information about the identities of the main bac- bohydrate polymers, carboxylic acid and amino terial players and their main organic substrates. acids (Sorokin, 1999;GroverandChrzanowski, Knowing which ‘bacteria’ use what sources of 2000; Søndergaard et al., 2000). ‘DOC’ sources is essential to the ecological inter- Though they may be unusable and unwanted pretation of the behaviour of pelagic systems. by theprimary producers, at least in the imme- Until quite recently, the identification of bac- diate short term, these organic solutes provide teria relied upon shape recognition, stain reac- aready and exploitable resource to pelagic bac- tion and substrate assay. Now, microbiology is teria (Larsson and Hagstrom,¨ 1979;Cole,1982; adopting powerful new methods for the isolation Cole et al., 1982;Selland Overbeck, 1992). The of nucleic acids (DNA and especially the 16S or existence of bacteria in the plankton, both free- 23S ribosomal RNA), their amplification through living and attached to small mineral and detri- polymerase chain reaction (PCR) and their match- tal particles in suspension, has for long been ing to primers specific to particular bacterial appreciated but, for many years, their role in taxa. The approach is similar for both marine doing much more than recycling organic detritus and freshwater bacterioplankton (good examples and liberating inorganic nutrients was scarcely of each are given by Riemann and Winding, 2001; appreciated. Interest in the ability of bacteria to Gattuso et al., 2002). Methods of enumeration assimilate the organic excretory products of pho- have advanced to routine automated counts by toautotrophs increased rapidly with the realisa- flow cytometry. The use of highly fluorescent tion that a large part of the flux of photosyn- nucleic acid stains makes for rapid and easy cyto- thetically fixed carbon is passed to the food web metric determination of microbe abundance and through a reservoir of DOC rather than through size distribution in simple bench-top apparatus thedirect phagotrophic activity of metazoans (Gasol and del Giorgio, 2000). In consequence, feeding onintact algal cells (Williams, 1970, the knowledge of the composition, abundance 1981;Pomeroy, 1974). It soon emerged that the and dynamics of planktic microorganisms is now chain of consumption of bacterial carbon – nor- developing rapidly. mally by phagotrophic nanoflagellates, then suc- In both lakes and the seas, the free-living cessively ciliates, crustacea and plantivorous fish heterotrophic bacteria occur in the picoplanktic –resultedinthetransfer of carbon to the higher size range (0.2–2 µm; <4 µm3), which they share trophic levels. This alternative to the more tra- with the photoautotrophic synechococcoids and ditional view of the pelagic alga → zooplank- eukaryote picophytoplankton (in lakes) and coc- ton → fish food chain soon became known as coid prochlorophytes (in the open ocean). Other the ‘microbial loop’ (Azam et al., 1983). Indeed, it keyparticipants in the oceanic microbial food now seems that the ‘loop’ is often the only viable webs (viruses, protists) are also prominently rep- means by which diffusely produced organic car- resented in those of lakes. These structural sim- bon can be exploited efficiently by the fauna of ilarities between marine and freshwater micro- resource-constrained pelagic systems. It is better bial communuties suggest that they both have CAPACITY, ACHIEVEMENT AND FATE OF PRIMARY PRODUCTION AT THE ECOSYSTEM SCALE 141

Ta b l e 3.4 Typical (upper) densities of bacterioplankton in lakes and seas and daily production rates.

Standing population Standing biomass Production (× 10−6 mL−1) (mg C m−3) (mg C m−3 d−1) Deep (>800 m) tropical 0.01–0.02 <0.4 <0.02 oceanic waters Surface tropical oceans 0.1–0.4 2–6 2–10 Oligotrophic lakes 0.5–0.8 8–15 4–12 Antarctic waters (summer) 1–2 20–60 ? Temperate ocean 1–2 20–70 10–50 Mesotrophic lakes 1–3 20–90 10–70 Inshore waters, estuaries 1.5–3 40–90 20–130 Oceanic coastal upwellings 2–5 90–500 40–150 Eutrophic lakes 3–8 150–500 70–150 Hypertrophic lakes, polluted 5–40 500–2500 120–700 lagoons

Source: Based on Sorokin, 1998. ancient and, possibly, common origins. The typi- primary production (GPP) rate of ∼230 mg C m−2 cal cell concentrations present in either broadly d−1 was considerably exceeded by bacterial respi- − fit within 2 orders of magnitude (105–107 mL 1), ration rate (1740 mg C m−2 d−1)but with little although pronounced seasonal variation is often change either to the bacterial abundance or to detectable, depending upon temperature, the the DOC pool (indicating almost no biomass accu- abundance of organic substrate and the inten- mulation and complete pelagic cycling of CO2). sity of bacterivorous grazing. It is clear that num- Significantly, an upwelling event, with a conse- bers generally reflect the trophic state and they quent pulse of nitrogen, stimulated GPP (to over are responsive to enhanced primary-producer 900 mg C m−2 d−1)and to the net recruitment activity (Nakano et al., 1998), especially in the through growth of phytoplankton, leading to an wake of phytoplankton ‘bloom’ periods (Coveney enhanced biomass of larger species ‘exportable’ and Wetzel, 1995; Sorokin, 1999; Ducklow et al., as food or in the sedimentary flux. The bacter- 2002)butthereisnoconstant proportionality. ial biomass decreased, relatively and absolutely, Indeed, relative to algal biomass, bacterial num- presumably in response to the rerouting of photo- − bers (104–107.6 mL 1:Vadstein et al., 1993; Sorokin, synthetic carbon. Where conditions are typically 1999)(seealsoTable3.4)diminish with higher more eutrophic, supporting biomasses of >2.5 nutrient availability (Weisse and MacIsaac, 2000). mg algal C L−1,bacterial mass may scarcely Using relationships resolved by Lee and Fuhrman exceed 0.5 mg C L−1. (1987)formarine bacterioplankton, heterotrophs The species structure of the bacterioplank- and photoautotrophs may each account for tonishighly varied and, collectively, includes − (roundly) up to 0.1 mg C L 1 of the phytoplank- species capable of oxidising substrates as varied tonbiomass of substantially oligotrophic sys- as carbohydrates, various hydrocarbons, proteins tems. Here, bacterial activity may exceed that and lipids (Perry, 2002). Presumably, the numbers of algae (Biddanda et al., 2001)and,thus, make of the particular types fluctuate in response to relatively the greatest contribution to organic- substrate supply and to grazing: distinct species matter cycling. In another recent study of the ‘successions’, in time and in space, have been carbon flux through the oligotrophic microbial demonstrated as the community composition community of the Bay of Biscay ([chla] < 0.7 mg responds to the dissipation of substrate pulses − m 3), Gonzalez´ et al. (2003)foundthat a gross moving through linear mainstem reservoirs (see 142 PHOTOSYNTHESIS AND CARBON ACQUISITION

especially Simekˇ et al., 1999). Interestingly, how- theproducers retain proportionately more photo- ever, the clearest trends in species composition synthate and invest it in the production of their seem to respond – like the phytoplankton itself – ownbiomass. to the availability of inorganic nutrients. Olig- In reality, planktic systems are rather more otrophic and mesotrophic assemblages in lakes complex than this simple model might indicate. (e.g. Simekˇ et al., 1999;Lindstrom,¨ 2000;Riemann One major distorting factor is the complicat- and Winding, 2001;Gattuso et al., 2002)andin ing and paradoxical role played by other, usu- the sea (Fuhrman et al., 2002;Cavicchioli et al., ally much more abundant, sources of dissolved 2003;Kuuppo et al., 2003; Massana and Jurgens,¨ organic matter in pelagic environments. In par- 2003)arecommonly dominated by species of ticular, dissolved humic matter (DHM) is often, the Cytophaga–Flavobacterium group and/or vari- by far, themajor component of the DOC con- ous genera of α-andγ-proteobacteria. It also tent of natural waters. Indeed, in the open ocean, seems likely that these are the main groups of where there is a fairly invariable base concentra- − bacteria colonising particulate organic detritus tion of ∼1mgL 1 of DOC (Williams, 1975; Sug- (Riemann and Winding, 2001), some of which imura and Suzuki, 1988), in lakes where concen- − anyway decomposes and disintegrates rapidly trations typically fall in the range, 1–10 mg C L 1 (Legendre and Rivkin, 2002a). The detailed stud- (Thomas, 1997), and in brown, humic waters ies of Cavicchioli et al. (2003)onthedynam- draining swamps and peatlands and in which − ics of the proteobacterium Sphingopyxis reveal humic matter accounts for 100–500 mg C L 1 therelevant properties of an oligotrophic het- (Gjessing, 1970;Freemanet al., 2001), DHM may erotroph. Besides its small size and high surface- represent some 50–90% of all the organic car- to-volume ratio, this obligately aerobic bacterium bon (including organisms) in the pelagic (Wetzel, has a high affinity for nutrient uptake. Pop- 1995; Thomas, 1997). The supposed origin of this ulation growth rates are sensitive to availabil- varied material – decomposing terrestrial plant ity of substrates (which include malate, acetate matter – is plainly self-evident in lake catch- and amino acids) and to the supply of inorganic ments, although neither the flux to the sea ions. nor its persistence in the ocean has been fully It is clear from this that, although plank- verified. tic photoautotrophs and heterotrophs have quite DHM has the reputation of resistance, independent carbon sources, they nevertheless or recalcitrance, to degradation by bacteria. have to compete for common sources of limit- Humic material appears in water as substances, ing inorganic nutrients. Moreover, it is likely that mainly phytogenic polymers, of relatively high the bacteria are superior in this respect (Gurung molecular weight and complexed with various and Urabe, 1999). Potentially, a mutualism devel- organic groups, which include acetates, formates, ops between nutrient-deficient autotrophs and oxalates and labile amino acids. By the time carbon-deficient heterotrophs. The elegant exper- they leach into water some decomposition has iments of Gurung et al. (1999)ontheplank- already taken place. The diversity of humic mate- tonofthe oligotrophic Biwa-Ko, Japan, illustrate rials, already large, is increased further (Wer- how this balance might be maintained. Under shaw, 2000): to make any kind of general assess- low light, photosynthesis is low and bacterial ment of the availability of DHM to pelagic bac- growth is constrained by low organic carbon teria is still difficult, awaiting more research. release. Increasing the light to nutrient-limited However, Tranvik’s (1998)thorough evaluation phytoplankton stimulates the supply of extra- of the bacterial degradation of DOM in humic cellular organic carbon and the growth of het- waters presents some well-considered analysis. erotrophs (and of their phagotrophic consumers). Many humic compounds are amenable to bac- Raising the resources available to the photoau- terial decomposition but, generally, the yield of totrophs, however, interferes with the organic energy to bacteria is rather poorer than non- carbon release to the increasing limitation of het- humic DOM. Most is relatively refractory but the erotroph production. With increased nutrients, resultant pools are not unimportant as bacterial SUMMARY 143 substrates, even though they turn over slowly. in pelagic bacterial biomass of 4.5 to 7.1 (Kirch- The rate of oxidation is influenced by the avail- man, 1990)are interpreted as being indicative ability of other nutrients, their tendency to floc- more of carbon than of nitrogen limitation of culate and their exposure to sunlight and photo- bacterial growth (Goldman and Dennett, 2000). chemical cleavage. This last turns out to be cru- Clearly, the relatively abundant forms of DOC cial, as the photodegradation of organic macro- in the oceanic pools often fail to satisfy the molecules to more labile and more assimilable requirements of the most abundant planktic het- products is now known to occur under strong erotrophs, which must therefore rely predomi- visible and ultraviolet irradiance (Bertilsson and nantly on the excretion of phototrophs, much as Tranvik, 1998, 2000;Obernosterer et al., 1999; the Gurung et al. (1999)model suggests. Equally Ziegler and Benner, 2000). As a result, many rela- clearly, it is a relationship of high resilience tively simple, low-molecular-weight organic radi- (Laws, 2003). cals may become available to microbes and may not necessarily be readily distinguishable from the DOM released by photoautotrophs (Tranvik 3.6 Summary and Bertilsson, 2001). The emphasis may still be on the restricted Pelagic primary production is the outcome of nature of the photodegradation and its confine- complex interplay among biochemical, physiolog- ment to surface layers, for the general impression ical and ecological processes that include pho- of slow decomposition of humic matter endures. tosynthesis and the large-scale dynamics of vari- It is likely that it is only in shallow-water sys- ous forms of carbon. Photosynthesis is the photo- tems where allochthonous inputs of DOM might chemical reduction of carbon dioxide to carbohy- sustain the predominantly hetertrophic activity drate, drawing upon radiant energy to synthesise that the relative abundance of organic carbon astore of potential chemical energy, pending its would lead us to expect. Elsewhere, it is mainly discharge when the carbohydrate (or its deriva- thenon-humic, autochthonously produced DOC tives) is oxidised (respiration). As in other pho- that seems likely to underpin heterotroph toautotrophs, algae and photosynthetic bacteria activity. employ two sequenced, chlorophyll-based photo- This last deduction fits most comfortably with systems. In the first, electrons are stripped from thepreviously noted general coupling between waterand transported to a reductant pool. In bacterial mass and primary production: the sup- thesecond, photon power re-elevates the electro- position that, on average, around half the pri- chemical potential sufficiently to transfer elec- mary production of the oligotrophic pelagic trons to carbon dioxide, through the reduction passes through the DOC reservoir requires that of nicotinamide adenine dinuceotide phosphate this must also be the more dynamic source of (NADP to NADPH). The carbon reduction process carbon and this supports the more active part of is built around the cyclical regeneration of ribu- bacterial respiration (Cole et al., 1988; Ducklow, lose 1,5-biphosphate (RuBP). RuBP is first com- 2000). Of course, the relationship is approximate, bined with (carboxylated) carbon dioxide and it is difficult to predict precisely and is plainly watertoform sugar precursors, under the con- subject to breakage. High rates of bacterivory, for trol of the enzyme RUBISCO, and from which instance, would cause one such mechanism. How- hexose is generated and RuBP is liberated (the ever, bacterial growth can become nutrient lim- Calvin cycle). The hexose may be polymerised (e.g. ited in very oligotrophic waters, to the extent to starch or glycogen) or stored. of positive DOC accumulation (Williams, 1995; The theoretical photosynthetic quantum yield Obernosterer et al., 2003), just as easily as it can is 1 mol carbon for 8 mol photon, or 0.125 mol be substrate limited in (say) nutrient-rich estu- C(mol photon captured)−1.Actual efficiency is aries (Murrel, 2003). In this context, it is espe- closer to 0.08 mol C (mol photon)−1,equivalent cially interesting to note the reports of oceanic to 2.821 kJ (mol C fixed)−1,or∼470 kJ (g C)−1. The microbiologistsreferringtoatomicC:Nratios maximum rates of photosynthesis are related to 144 PHOTOSYNTHESIS AND CARBON ACQUISITION

therate of electron clearance from the reductant recycles. Indeed, most smaller lakes probably pool (and which responds to the photon flux), release more CO2 to the atmosphere than they as well as to an adequate supply of CO2 to the take from it. They are considered to be net het- RUBISCO reaction (if a concentration of >0.01 erotrophic. Only in very large, oligotrophic sys- mM is not maintained, the enzyme acts as an tems does the sedimentary export of carbon bal- oxygenase). ance the atmospheric inorganic uptake flux (at Physiologically, photosynthetic rate is sensi- some 50–90 g C m−2 a−1). tive to temperature, to light and carbon dioxide Globally, pelagic photosynthesis accounts for availability. Evenat30◦C, given saturating light around 45% of the planetary carbon fixation. and an adequate carbon supply, photosynthesis In some circumstances, when photosynthesis is achieves <20 mg C (mg chla)−1 h−1. Maximum constrained (especially by light dilution) the photosynthetic rates are generally halved for each carbon is invested in the growth of the pho- 10 ◦Cdrop in temperature. Below saturation (usu- toautotroph. These organisms become potential ally <150 mol photons m−2 s−1), photosynthetic food to pelagic grazers. In many other cases, ratesfall in a light-dependent manner, in the pro- light saturation or nutrient depletion result in portion 6–18 mg C (mg chla)−1 (mol photon)−1 carbon fixation in excess of contemporaneous m2.Carbondioxide concentrations below air growth requirements and photosynthate is either saturation may also limit photosynthetic rates. reoxidised or excreted as dissolved organic car- Some algae are extremely efficient in adapting bon (DOC). This augments an already relatively to photon harvesting under very low light fluxes large pool of dissolved humic matter (DHM) but or in the fluctuating light experienced by phy- presents a much more amenable substrate for toplankton entrained in mixed water columns. pelagic bacteria. Like those of photoautotrophs, Some algae are restricted to carbon dioxide as concentrations of heterotrophic bacteria reflect a carbon source and are sensitive to the very theavailability of inorganic nutrients and there low concentrations experienced at pH >8. Others is mutual competition. However, bacterial growth can use bicarbonate or employ energy-consuming is often more carbon limited while the main carbon-concentrating mechanisms to focus the producers are usually nutrient limited. Besides limited fluxes at the sites of synthesis. In this themutualism that this situation engenders, way, low light and low carbon availability select the acquisition by bacteria of organic carbon strongly for well-adapted species. products of the phytoplankton and the con- On a local basis, it is possible to calculate sumption of bacteria by microzooplankton rep- the carrying capacity of the environment and resents the main route of pelagic photosynthate the rates of biomass assembly that might be sus- to thepelagic food web. This ‘microbial loop’ tainable. Down-mixing and light dilution place commonly dominates the first steps in the food important limits on both. The carbon flux from chain, is certainly of great antiquity, and should the atmosphere is potentially – and, at times, no longer be regarded as a special exception to is – a constraint on area-specific photosynthe- alga–herbivore–fish linkages. It is the latter that sis but is avoided in most lakes and at most are the exception, being sustainable only in rela- times by inflowing CO2-saturated and internal tively resource-rich conditions. Chapter 4

Nutrient uptake and assimilation in phytoplankton

There is a huge literature on this topic. The 4.1 Introduction purpose here is not to review the findings in detail or to give more than the sketchiest outline This chapter addresses the resource requirements of the historical development of the understand- forthe assembly of photoautotrophic biomass. In ing of nutrient limitation. Even the elements addition to light and carbon, growth of phyto- most often implicated in the constraint of phytoplankton consumes ‘nutrients’ and, equally, may plankton growth (nitrogen, phosphorus, iron and often be constrained by their availability and one or two other trace elements, together with fluxes. Put at the most basic level, every repli- thewell-known constraint on diatom growth set cation of a phytoplankton cell roundly demands by its skeletal requirement for considerable quan- theuptake and assimilation of a quota of (usu- tities of silicon) are sufficiently well and clearly ally) inorganic nutrients similar to that in the known not to require any long and detailed mother cell, if her daughters are to have the account of how this recognition came about. The similar composition. Ignoring skeletal biominer- approach that I have adopted is first to consider als for the moment, we may recall fromSec- the mechanisms of nutrient uptake and the gen- tion 1.5.3 that, in addition to carbon, the liv- eral constraints that govern the successful assimi- ing protoplast comprises at least 19 other ele- lation and anabolism of resources by phytoplank- ments. Some are needed in considerable abun- ton. Then, mainly by reference to the key limiting dance (hydrogen, oxygen, nitrogen), others in elements (N, P, Fe, etc.), I seek to show how the rather smaller amounts (phosphorus, sulphur, abilities of phytoplankton to gather the resources potassium, sodium, calcium, magnesium and necessary to support cell growth and replication chlorine), for the assembly and production of might impinge upon the dynamics and ecology theorganic matter of protoplasm. Others occur of populations. as vital traces in support of cellular metabolism Uptake and assimilation of these nutrients do (silicon, iron, manganese, molybdenum, copper, need to be considered in rather more detail, as cobalt, zinc, boron, vanadium). However, it is impairment to these processes, mostly through less the amounts in which these elements are resource deficiencies, is frequently implicated in required that constrains growth than does the the comparative dynamics and relative abun- ease or otherwise with which they are obtained. dance of phytoplankters. It is important to It is the demand (D)relative to the supply (S) recognise that the first impediment to be overthat is ultimately critical, bearing in mind that a come is that just about all of the nutrients measurable presence is not a measure of avail- to be drawn from the water occur in concen- ability if the element in question is not both trations that, relative to their effective concen- soluble and diffusible and, so, assimilable by trations within the cell, are extremely dilute, cells. or rarefied. How these steep gradients are 146 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

overcome is an appropriate starting point for our sites of their anabolism into proteins and, even- consideration. tually, into organelles. The cell is ordered, with relative compositional homeostasis based on balanced resource deployment and controlled com- 4.2 Cell uptake and intracellular position. Outside the cell, the external medium transport of nutrients is chaotic: besides signalling irregular and rapid fluctuations in the photon flux, the solutes to which the cell is exposed are often patchily dis- To describe adequately the main structures of tributed, even at the scale of a few millimetres. aeukaryotic unicellular phytoplankter that are Some initial calculations illustrate the mag- involved in the uptake, transport and assembly nitude of the uptake requirement. Starting from of inorganic components, it is helpful to refer thepremise that the ash-free dry mass of the to the simplified and stylised diagram in Fig. 4.1. cytoplasm accounts for between 0.41 and 0.47 Inside the multiple-layered plasmalemma (shown pg µm−3 of live volume and that between 46% as a single line), there is a nucleus contain- and 56% of the ash-free dry mass is carbon, then ing the genomic proteins (marked ‘DNA’); the it follows that the carbon concentration in the ribosomal centres of protein synthesis are rep- replete, healthy, live cell is in the range 0.19 to resented by ‘RNA’ and part of the structure of 0.26 pg C µm−3,or225 ± 35gCL−1. This is thechloroplast and the thylakoid membranes equivalent to 18.8 mols C L−1.Against the air- are also sketched. Superimposed upon the cell is equilibrium concentration of carbon dioxide in aseries of arrows that provides a fragmentary water (0.5–1 mg L−1,orbetween11 and23µmol indication of the key pathways located within L−1), the growing cell is literally accumulating the protoplast. The arrows refer, in part, to the carbon atoms against a concentration gradient dynamics of photosynthetic reduction of inor- in the order of 1 000 000 to 1. Moreover, in order ganic carbon dioxide and, in part, to the uptake to accomplish a doubling of cell material, it has and intracellular delivery of key nutrients to the to acquire another 1 mol carbon for every 1 mol of carbon in the newly isolated daughter tissue. The corresponding calculations for the average cell concentrations of nitrogen (∼2.8 mols N L−1) and phosphorus (∼0.18 mols P L−1)areofasimi- lar magnitude greater than they might typically occur in natural waters (2–20 µmol N L−1; 0.1–5 µmol P L−1). In relation to the carbon requirement, each cell has to draw on the equivalent of ∼151 mmolNand 9.4 mmol P for each mol of C required to replicate the cell mass.

4.2.1 Supply of nutrients Based on the example of carbon, the well- developed nutrient harvesting capabilities of algae have already been indicated (see, especially, Section 3.4.2). However, it is not simply a matter ofengineering a high afﬁnity for the carbon dioxide (or, indeed, other nutrient in the adja- Figure 4.1 Diagram of a phytoplankton cell to show the cent medium) as the mechanisms can only be essential pathways for the gathering and deployment of the effective over a short distance beyond the cell. keyresources. Based on an illustration of Harris (1986) and The operational beneﬁts are really restricted to reproduced with permission from Reynolds (1997a). within the boundary layer adjacent to the cell. CELL UPTAKE AND INTRACELLULAR TRANSPORT OF NUTRIENTS 147

Here, the movement of solutes are subject to Fick- where t is time, m is the coefficient of molecular ian laws of diffusion (cf. Eq. 3.19). The renewal, diffusion of the solute (as in Eq. 3.19)andN = or replenishment, of nutrients in this immedi- (δ/δx, δ/δy, δ/δz)isanintegral of the gradients in ate microenvironment of the cell can also be the x, y and z planes. Supposing steady state in a critical and, hence, so is any attribute of the symmetrical sphere, this will reduce to: organism that enhances the rate of entry of d/dr r 2dC /dr = 0 (4.2) essential solutes into that boundary layer. Such b b b adaptations in this direction may raise directly where rb is the radial distance from the centre the effectiveness of nutrient gathering by the of the sphere. It may be solved for the space to cell. theedge of the boundary, Csurface = C(rb = a), and The importance of the movement of water beyond, Cbulk = C(rb →∞), so that: relative to the phytoplankter (or, as we now = − − / recognise, to the phytoplankter plus its bound- C (rb) C bulk (C bulk C surface)a rb (4.3) ary layer) was famously considered by Munk and The flux (Fa)ofthe solute to the cell is calculable Riley (1952). They were among the firsttopoint as: out that the effect of motion – either active = π 2 / | ‘swimming’ or passive sinking or flotation – is F a 4 a mdC drb rb=a to increase the solute fluxes to the cell above = 4πam(C bulk − C surface) (4.4) those that would be experienced by one that is non-motile with respect to the adjacent medium. If the live cell now retains the inwardly diffusing This seemingly axiomatic statement was verified solute molecules, Csurface diminishes to zero and through the experiments of Pasciak and Gavis the flux increases towards a maximum:

(1974, 1975)andtheinterpolation of the results F amax = 4πamC bulk (4.5) to the benefits to nutrient uptake kinetics of adiatom of sinking through nutrient-depleted The effect of the motion of the cell, sinking, float- water. In consideration of these data, Walsby ing or ‘swimming’ through water is to increase and Reynolds (1980) determined the trade-offs the flux to the diffusive boundary layer at the between sinking and uptake rates in sinking same time as compressing its thickness (Lazier diatoms: there was always a positive benefit in and Mann, 1989). The distribution of a nutrient material delivery but at the ambient external solute next to the cell is modified with respect to concentrations critical to sufficiency, the com- Eq. (4.1)bythe advection owing to the hydrody- pensatory sinking rates become unrealistically namic flow velocity, u: large. In other words, motion relative to the δ /δ + = 2 C t u NC m( N) C (4.6) medium undoubtedly assists the renewal and delivery of nutrients to the immediate vicinity The advection–diffusion equation is not easily of the plankter but, ultimately, is no guarantee soluble. The approach of Riebesell and Wolf- of satisfaction of the plankter’s requirements at Gladrow (2002)wastorewrite the problem in low concentrations. dimensionless Navier–Stokes terms, using parti- Amodern, empirical perspective on this topic cle Reynolds (Section 2.3.4 and Eq. 2.13), Péclet has been pursued in the work of Wolf-Gladrow and Sherwood numbers. The Péclet number (Pe) and Riebesell (1997;seealso the review of Riebe- compares the momentum of a moving particle sell and Wolf-Gladrow, 2002). Starting from the to diffusive transport. For a phytoplankton cell perspective of the single spherical algal cell with whose movement satisfies the condition of non- an adjacent boundary layer of thickness a,the turbulent, laminar flow (Re < 0.1; Section 2.4.1), concentration (C)ofagivennutrient in the imme- − Pe = (u d) m 1 (4.7) diate microenvironment is subject only to diffu- s sive change, in conformity with the equation: where us is the intrinsic velocity of a spherical cell of diameter d.Inthe present context, where 2 δC /δt = m(N) C (4.1) theparticle is introduced into the flow field u 148 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

influence of the turbulent shear rate (Karp-Boss et al., 1996). They showed: Sh = 1.014 + 0.015Pe2 (4.9) when the Péclet number was derived from: Pe = (d/2)2 (E /ν)2 m−1 (4.10) in which equation, d is the diameter of a spherical cell, E is the turbulent dissipation rate, in m2 s−3, ν is the kinematic viscosity of the water (in m2 s−1)andm is the coefficient of molecular diffusion of the solute (for further details, see Section 2.3.3). A further deduction and reinterpretation of the comment of Walsby and Reynolds (1980;see Figure 4.2 The Sherwood number as a function of the above) is that relative motion does not in itself Péclet numbers for steady, uniform flow past an algal cell overcome rarefied nutrient resources. However, (solid line) and turbulent shear (dashed line). Figure redrawn chronic and extensive resource deficiencies must with permission from an original in Riebesell and exact a greater dependence of larger algae on tur- Wolf-Gladrow (2002). bulence to fulfil their absolute resources requirements to sustain growth requirements than they do of smaller ones. Conversely, smaller cells (x, y, z, Re), the Pécletnumberalsoexpressesthe are less dependent upon turbulent diffusivity ratio of the scales of advective (u N C)anddif- to deliver their nutrient requirements than are 2 fusive solute transport (m( N) C). The Sherwood larger ones. number (Sh)istheratio between the total flux of anutrient solute arriving at the surface of a cell 4.2.2 Moving nutrients into the cell in motion and the wholly diffusive flux. Riebesell The transfer of nutrients from the enveloping and Wolf-Gladrow (2002)showed that, for parti- boundary layer into and within the cells is cles in motion with very low Reynolds numbers, biologically mediated, being effected principally Sherwood numbers are non-linearly related to through a series of substance-specific membrane Péclet numbers but, in the range 0.01 ≤ Pe ≤ 10 transport systems. Modern molecular biology is (which embraces the sinking motions of algae providing the means to investigate both the from Chlorella to Stephanodiscus;seeSection 2.4.1), mechanisms by which cells marshal and assem- the relationship is adequately described by: ble components in cellular synthesis and how Sh = 2 + 2(1 + 2Pe)a (4.8) their operations are regulated. In the case of membrane transport systems, working against a The relationship (sketched in Fig. 4.2)shows concentration gradient, structure and function that, for small cells embedded deeply in the tur- conform to a generalised arrangement common bulence spectrum (Pe < 1), the benefit in terms to most living cells. In essence, these accept spe- of nutrient supply is marginal (Sh ∼1). For larger cific target molecules and transfer them to the units and motile forms generating Re > 0.001 and sites of deployment. These movements are gener- Pe > 1, the dependence on turbulence for the ally not spontaneous and, so, require the expen- delivery of nutrients becomes increasingly signif- diture of energy. Power, fuelled by ATP phosphor- icant (Sh > 1). ylation, is used to generate and maintain ion The conclusion fits comfortably with the gradients and proton motive forces, through the demonstration of a direct relationship of algal coupling of energy-yielding reactions to energy- size to Sherwood scaling, mediated through the consuming steps (Simon, 1995). CELL UPTAKE AND INTRACELLULAR TRANSPORT OF NUTRIENTS 149

torbythe reaction with the target becoming the excitation of the next. The sequenced reactions of thetransporter proteins provide a redox-gradient ‘channel’ along which the target molecule is passed. The whole functions rather like a line of people helping to douse a fire. The first lifts the filled bucket and passes it to the next, who, in turn passes it to a third. Only after the second has accepted a bucket from the first can the first turn to pick up another bucket. The second cannot accept another bucket until he has passed on the last and is once more receptive to the next. In much the same way as the fire-fighters might be supplied with filled buckets more rapidly than they can be dispatched down the line, so the molecular sequence can become saturated and the fastest rate of uptake then fails to deplete the supply of target nutrients. At theother extreme, exhaustion of the immedi- Figure 4.3 Basic structure of a receptor–excitation ate source of buckets or targets leaves the entire assembly, used to capture, bind and transport specific target molecules into and within the phytoplankton cell. Based on a sequence idle but the full transport capacity figure in Simon (1995) and reproduced with permission from remains ‘open’ and primed to react to the stimu- Reynolds (1997a). lation of the next arriving molecule. The activity state of the transport system is communicated to the controlling genes. It is In the specific case of nutrient uptake, the extremely important that the cell can react to linkages involve sequences of protein–protein thesymptoms of shortages of supply (of, say, interactions in which the binding of a spe- phosphorus) by regulating and closing down the cific target ligand at a peripheral receptor stim- assembly processes before the supply of compo- ulates an excitation of the transfer response. The nents (or a particular component) is exhausted. basic structure of the transmembrane assembly What happens is that a second group of regu- is sketched in Fig. 4.3. The receptor region is latory proteins associated with the transporters periplasmic and constitutes the ligand-specific activate the transcription of particular genes protein. Reaction with the target molecule stimu- called operons. While the uptake and transport lates a molecular transformation, which, in turn, mechanism is functioning normally, the operons becomes the excitant substrate to the proteins repress the expression of further genes which of the transmembrane region. The central reac- regulate the reactions to nutrient starvation tion within this complex is to catalyse the phos- (Mann, 1995). For instance, an external shortage phorylation of the substrate. This is, of course, of a given nutrient (say, orthophosphate ions) theprincipal reaction through which cells regu- will result in a diminishing frequency of recep- late the transfer of redox power. The high-energy torreactions and a weakening suppression of the pyrophosphate bond between the second and genes that will activate the appropriate cellular third radicals of ATP is broken by a kinase, the response. The response may be to produce more conversion to the diphosphate releasing some phosphatases or to promote the metabolic close- 33 kJ (mol)−1 of chemical energy. down of the cell, including entry into a resting The further proteins in the series react analo- stage, before thecellstarvestodeath(seealso gously and sequentially, the excitation of a recep- Sections 4.3.3, 5.2.1). 150 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

4.2.3 Empirical models of nutrient uptake Many of the well-established paradigms relating to the uptake and deployment of nutrients and the ways in which these impinge upon the growthanddynamics of phytoplankton are founded on a welter of experimental observations. However, it is a small number of classic studies that have provided much of the insight and understanding, into which the majority of observations can be interpolated. For instance, themodel of Dugdale (1967)recognised the Figure 4.4 Uptake rates of molybdate-reactive phosphorus saturable transport capacity (corresponding to by cells of Chlorella sp., pre-starved of phosphorus, as a the fully ‘open’ condition of the receptors) and function of concentration, according to data of Nyholm the simultaneous dependence of the rate of (1977). Redrawn with permission from Reynolds (1997a). uptake upon resource availability in the adjacent medium. Dugdale showed that the relationship between the rate of uptake of nutri- found to be less satisfactory for the descrip- ents in starved cells and the concentrations in tion of nutrient-limited growth rates. This may which the nutrient is proffered conforms to be attributed, in part, to inappropriate applica- Michaelis–Menten enzyme kinetics, as expressed tion and a misplaced assumption – analogous to by the Monod equation. Dugdale’s (1967)general theone about photosynthesis and growth – that equation stated: growth rates are as rapid as the relevant materials can be assembled. In fact, growing cells may = / + VU VUmax S (K U S) (4.11) take up nutrients when they are abundant much more rapidly than they can deploy them, just as The equation recognises that the rate of uptake they can sustain growth at the expense of inter- of a nutrient by fully receptive cells is a func- nal stores at times when the rate of uptake may tion of the resource concentration, S,uptoa be constrained by low external concentrations.

saturable limit of VUmax . KU is the constant of Droop (1973, 1974)cleverly adapted the Dugdale half saturation (i.e. the concentration of nutri- model to include a variable internal store in ent satisfies half the maximum uptake capacity). order to represent the impact of the cell quota There is no way to predict these values accu- on the rate of growth. The impacts of nutrient rately save by experimental determination. Many deficiencies on cell replication are considered in measurements show close conformity to the pre- Chapter 5 (see Sections 5.4.4, 5.4.5). However, it is dicted behaviour and, hence, to the generalised useful to introduce here the concept of an inter- plot in Fig. 4.4,showing the uptake of phospho- nal store in the context of its influence on uptake rus by Chlorella,asdescribed by Nyholm (1977). and, indeed, its relevance to how we judge ‘lim- Because the uptake rates and affinities are, how- itation’ and its role in interspecific competition ever, very variable among individual phytoplank- for resources. ton species,theyaremostconveniently intercom- It is, firstly, quite plain that the intracellular pared by reference to the magnitudes of alga- content of the cell starved of a given particular

and nutrient-speciﬁc values of VUmax and KU.For resource will not just be low (leaving the cell very

instance, a relatively high VUmax capacity com- responsive to new resource) but it will probably bined with a low KU is indicative of high uptake be close to the absolute minimum for the cell to affinity for a given nutrient. stay alive. This is Droop’s ‘minimum cell quota’ The Monod model has been widely applied (q0)andit is too small to be able to sustain any and found to describe adequately the uptake growth. Secondly, raising the actual internal con- by algae of essential micronutrients, under the tent (q) above the minimal threshold (essentially starvation conditions described. It has been through uptake) makes resource available to PHOSPHORUS 151 deployment and growth. At low but steady rates theliterature. In the following considerations, of supply, some proportionality between the rates theusage is necessarily precise, adhering to the of growth (r )andresource is expected to be evi- definitions shown in Box 4.1. − dent. Interpolating (q q0)forS, r for VU and rmax for V in Eq. (4.11), the Droop equation states: Umax 4.3 Phosphorus: requirements, = − / + − r rmax(q q0) (K r q q0) (4.12) uptake, deployment in As it cannot be assumed that growth and uptake phytoplankton are half-saturated at the same concentration, we must also substitute a half-saturation con- The phosphorus relations of phytoplankton cells stant ofgrowth, (Kr). By analogy, we might also provide a good example of the ways in which assume that, again at a low but steady rate of the adaptations for gathering of an essential supply, r and V and r and V are mutu- U max Umax but frequently scarce resource impinge upon ally interchangeable. Such equivalence is demon- thedynamics of populations and the species strable, provided the steady-state condition holds structure of natural assemblages. As a compo- (Goldman, 1977;Burmaster, 1979). However, nent of nucleic acids governing protein synthesis when supply rates exceed deployment and the and of the adenosine phosphate transformations internal store increases, the uptake rate must that power intracellular transport, phosphorus slow down, even when a high external concen- is an essential requirement of living, functional tration obtains. It might then be proposed that plankters. As observed earlier (Section 1.5.3), the nutrient uptake is better described by: phosphorus content of healthy, resource-replete, actively growing phytoplankton cells is generally VU = [(qmax − q)/(qmax − q0)] close to 1–1.2% of ash-free dry mass (Round, 1965; [V S/(K + S)] (4.13) Umax U Lund, 1965), with a molecular ratio to carbon of around 0.0094 (106 C : P). The minimum cell where (qmax)isthereplete cell quota. The larger is the instantaneous cell quota, q,thesmaller quota (q0)may vary intespecifically, most proba- will be the effective rate of uptake. The mul- bly, between 0.2% and 0.4% of ash-free dry mass tiple allows the cell to accumulate even scarce (some 320–640 mol C : mol P) but, reportedly, resources (of, say, phosphorus) from low concen- almost an order lower in some species (Asteri- ∼ trations so long as the uptake of another (say, onella 0.03% of ash-free dry mass: Rodhe, 1948; nitrogen) is controlling (‘limiting’) the rate of the Mackereth, 1953), equivalent to molecular C : P ∼ deployment of both in the structure of new cell ratios of 4000). Conversely, intracellular stor- material. An independent increase in the supply age capacity of phosphorus may allow q to rise ≥ ≤ of the second resource (nitrogen), however, with in some species to 3% of dry mass ( 40 C : P). no simultaneous alteration in the availability of The interesting deduction is that, as a result of the first(phosphorus), might very quickly leave this so-called ‘luxury uptake’, the cell may con- therate of supply of the first as the limiting contain 8–16 times the minimum quota and that, straint, when the internal quota is likely to be as a consequence, it is theoretically able to sus- drawn down. This principle underpins the use of tain three or possibly four cell doublings without intracellular nutrient ratios to indicate the nutri- taking up any more phosphorus. ent status of cells and, thus, the identity of the instantaneously ‘limiting factor’. Interspecific dif- 4.3.1 The sources and biological availability ferences in the competitive abilities of algae to of phosphorus in natural waters function at low resource availability are also held The natural sources of phosphorus in water are to influence the structure of communities. thesmall amounts that occur in rainfall (gen- The terms ‘limitation’ and ‘competition’ (in erally 0.2 to 0.3 µM), augmented by phosphates the context of satisfying resource requirements) derived from the weathering of phosphatic min- have been used variously and inconsistently in erals, especially the crystalline apatites, such 152 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

Box 4.1 Limitation and competition in the nutrient relations of phytoplankton

The word ‘limitation’ has been used, variously, to explain the control of phytoplankton growth dynamics, the poverty of plankton biomass and the dearth of the supportive nutrients. All non-toxic environments have a ﬁnite supportive capacity, which is generally based upon the notion that available resources are deployed in

the assembly of biomass, ideally, in quasi-ﬁxed quotas, up to a maximum, Bmax =

Ki/q0, where = Ki is the steady-state concentration of the ith resource and q0 is the minimum cell quota in the biomass, supposing a uniform, Redﬁeld-type composition, or the minimum cell quota in the biomass of the jth species. In this usage,

the limiting capacity is the lowest of the individual supportive capacities, Ki.Byimpli- cation, the ratios among the components of the cell will show supra-ideal values to the one that is sub-ideal and, thus, biomass limiting (Reynolds, 1992a; Reynolds and Maberly, 2002). The capacity limitation by the factor least available relative to demand is the expression of von Liebig’s ‘Law of the Minimum’ (von Liebig, 1840). In practical terms, the identity of the capacity-limiting factor is revealed by the magnitude of the response to its augmentation. Gibson (1971) usefully deduced that a substance is not capacity-limiting if an increase in that factor produces no stimulation to the biomass that can be supported. Growth dynamics may also limited, in the sense that the rate of biomass elaboration is determined by the rate of resource supply. Moreover, the rate-limiting factor is the one upon by whose rate of supply determines the rate of elaboration. Analysing data on the growth of the diatom Asterionella in Windermere over a period of 50 years, Reynolds and Irish (2000)were able to confirm Lund’s (1950) view that the biomass capacity was set by the winter concentration of soluble reactive silicon. However, they also showed that the rate of its attainment had been phosphorus limited and that the timing of the silicon-limited maximum had advanced over the period of the documented enrichment of available phosphorus in this lake. ‘Competition’ is used inconsistently by biologists. However, the term ‘competitor’ is applied by aquatic ecologists, with great consistency, to refer to species that eventually rise, tortoise-like, to a steady-state dominance. Unfortunately, in the parlance of terrestrial plant ecologists, a good competitor is dynamic, fast-growing and applicable to Aesop’s fabled hare. Mindful of the place that competition theory occupies in ecological and evolutionary theories, it seems important to have robust definitions. In this book, I use ‘competition’ in the sense of Keddy’s (2001) definition as ‘The negative effects that one organism has upon another by consuming, or controlling access to, a resource that is limiting in its availability.’ Thus, a competitive outcome has only transpired if the activities of species 1 denies access to the resources required to nourish the activities of species 2. Being able to grow faster when fully resourced does not, by itself, make species 1 ‘more competitive’ than species 2. It is merely more efficient in converting adequate resources into biomass. On the other hand, the behavioral or physiological flexibility of species 2tobetter exploit a critically limiting resource affords a significant competitive advantage over species 1, at such times when that resource limitation is operative. PHOSPHORUS 153 as fluorapatite and hydroxylapatite, and the ganese), although there is the further complica- amorphous phosphorite. All are forms of calcium tion of their redox sensitivities. At redox poten- phosphate, which has a low solubility in water tials below +200 mV, the higher-oxidised ion, at neutrality, and the bioavailability of phospho- Fe3+,isreduced to the divalent Fe2+. Whereas the rus indrainagewaterstends to be low (Emsley, hydrolysis of the trivalent ion leads to the precip- 1980). Terrestrial plants and the ecosystems of itation of insoluble ferric hydroxide, divalent fer- which they are part share analogous problems rous ions remain in solution. Raising the redox of phosphorus sequestration. Not surprisingly, potential favours the opposite reaction (Fe2+ − forested catchments, especially, remove and accu- e → Fe3+,although it is usually enhanced by mulate much of the modest quantities of inor- microbial oxidation): the floccular ferric hydrox- ganic phosphorus with which they are supplied, ide precipitate scavenges orthophosphate ions, leaving little in the export to receiving waters again in exchange for hydroxyls. At close to neu- save as organic derivatives of biogenic products. trality, the orthophosphate ions are substantially The losses of inorganic phosphorus to water immobilised (‘occluded’) to the extent that they can be greatly enhanced through anthropogenic are scarcely any longer available to algal or micro- activities (quarrying, agriculture and tillage and, bial uptake. Only a further change in redox or especially, the treatment of sewage) but the gen- an increase in the ambient alkalinity of the eral condition of natural waters draining from medium alters this position. The phosphate ions any but desert catchments and/or ones with an that are released into solution are, potentially, abundant occurrence of evaporite minerals is to fully bioavailable (Golterman et al., 1969). be moderately or severely deficient in inorganic Redox-mediated changes in phosphate solubil- phosphorus (Reynolds and Davies, 2001). ity in sediment water and in limnetic hypolimnia In all its biologically available (or ‘bioavail- were described over 60 years ago (Einsele, 1936; able’) forms, phosphorus occurs in combination Mortimer, 1941, 1942). Since then, many of the with oxygen in the ions of orthophosphoric fears about the impacts of phosphorus enrich- acid, OP(OH)3 (Emsley, 1980). Orthophosphoric ment on aquatic ecosystems have continued to acid itself is a weak tribasic acid and is freely be dominated by the renewed bioavailability water soluble. The relative proportions of the to phytoplankton of sediment phosphorus. Of 3− 2− − various anions (PO4 ,HPO4 and H2PO4 )vary course, there still needs to be phytoplankton with pH. The hydrogen radicals are all replace- access to these phosphorus sources. Though the able by metals. The orthophosphates of the ‘release’ of orthophosphate to the water seems alkali metals (except lithium) are also solu- just as likely an occurrence, most of this should ble but those of the alkaline earth metals be re-precipitated with ferric iron, once the and the transition elements are quite insolu- redox is raised sufficiently (≥+200 mV). Under ble. Three of these – calcium, aluminium and severe reducing conditions (redox potential ≤ iron – are especially relevant to the consider- −200 mV), however, sulphate ions are reduced to ation of phosphorus availability and plankton sulphide ions. These readily precipitate with fer- behaviour. The precipitation of calcium phos- rous iron, thus scavenging the water of Fe2+ ions. phate effectively removes orthophosphate ions The consequence then is that, on re-oxidation, from solution, in stoichiometric proportions. The theresidual iron content will be diminished, less bioavailability of orthophosphate ions can be sig- ferric hydroxide will precipitate and less phos- nificantly affected through exchange with the phate may be scavenged. High phosphate levels in hydroxyl ions that are otherwise immobilised, eutrophic systems may be more influenced by the in large, non-stoichiometric numbers, on the redox transformations of sulphur than by those surfaces of aluminium oxides; this sorption of of iron. the orthophosphate ions effectively renders them Certainly, the solubility transformations at biologically unavailable. A similar behaviour high pH and the behaviours of other elements characterises the reactions of phosphate with at low redox can have profound effects on the the precipitated hydroxides of iron (and man- bioavailability of phosphate in natural waters 154 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

Ta b l e 4.1 Phosphorus-containing fractions in water: nomenclature and availability

Phase Abbreviation Chemical sensitivity and bioavailability Dissolved P DP Free orthophosphate ions, some in combination with organic derivatives. Assumed to be freely bioavailable Soluble, MRP (or SRP) DP + ﬁne colloidal organic material. molybdate-reactive P Demonstrably bioexhaustible and supposed to be freely bioavailable Particulate P PP Phosphorus not in solution or in ﬁne colloids but bound to suspended solids; fraction subdivisble as: Water-extractable PP IMRP Phosphorus moves into solution in irrigating water; most frequently encountered in intact sediments, where it is mainly from the interstitial and is conditionally bioavailable NH4Cl-extractable PP NH4Cl-P Particle-bound phosphorus, ion exchangeable and conditionally bioavailable Citrate-dithionate- Na2S2O4-P Iron-bound phosphorus. Scarcely bioavailable, extractable PP dependent upon low redox or high pH NaOH-reactive P NaOH-rP Iron- and aluminium-bound phosphorus, sensitive to high pH. Otherwise scarcely bioavailable Non-alkali-reactive PP NaOH-nrP PP that is not soluble in strong alkali; fraction includes: HCl-reactive P HCl-P Phosphorus in compound with alkaline metals, esp. apatite. Scarcely bioavailable non-HCl-reactive resP (Organic) PP soluble only in powerful oxidant residue (e.g. perchloric acid). Not bioavailable HClO4-digestible P TP Perchloric acid digestion releases all known combinations of phosphorus. Phosphorus quoted as ‘TP’ is only partially bioavailable as roughly determined by serial analysis of the above sequence

Source: Based on Table 1 of Reynolds and Davies (2001), compounded from various sources.

(Lijklema, 1977). On the other hand, the mecha- eral and biogenic particulate phosphorus in the nisms favouring increased bioavailability of phos- water) generally under 1–2 µM. Moreover, only phorus are more active in environments that are asmall proportion of this TP may be in solu- already relatively enriched with respect to this tion or be so readily soluble to be measurable by and other nutrients. These are not exceptional or the standard molybdenum-blue method of Mur- uncommon conditions among shallow, enriched phy and Riley (1962). Most of the balance will lakes. However, the wide acceptance that a major- already be constituent in pelagic biomass or in ity of lakes and many seas conform to a model of non-bioavailable colloids and fine particles. pristine conditions characterised by low phospho- These various fractions are potentially sep- rus availability is well justified. Such habitats fre- arable by serial assays, each step using a pro- quently carry a total-phosphorus concentration gressively more aggressive chemical cleavage (TP, being the aggregate of all dissolved, min- (see Table 4.1). Prior to these methods being PHOSPHORUS 155 developed, the understanding of phosphorus phosphorus. One of these, a 32-kDa polypep- dynamics was poised between the detection of tide, was localised in the cell wall, linked to small amounts of molybdate-reactive phosphorus an intracellular 100-kDa polypeptide. Together, (MRP), with poor sensitivity, and the MRP con- these conform to the typical structure of a recep- tent of companion samples after digestion with tortransport system (cf. Fig. 4.3). These polypep- powerful oxidants, supposedly corresponding to tides showed 35% identity and 52% similarity the TPconcentration. Neither necessarily affords with those of E. coli. They also showed that the aclearnotion of the supportive capacity of the encoding genes were almost identical to those bioavailable forms (BAP): the MRP content, if reli- isolated from other Synechococcus strains, which ably measurable at all, is an underestimate of had already been linked to the induction of phos- BAP, with some or most of what is available hav- phatase activity in Synechococcus PCC7942 (Ray et ing already been biologically assimilated. The TP al., 1991). Alkaline phosphatases are a well-known determination is always likely to include frac- group of zinc-based enzymes which break phos- tions that are chemically immobilised and, in phate ions from organic polymers in the external theshort term, biologically inert. The whole issue medium close to the cell. These are also said to of what is or is not bioavailable is complex and be produced only under conditions of declining requires a different approach (see Section 4.3.2). external orthophosphate concentrations. Ihlen- Yet itisperfectlyclear, from studies of systems as feldt and Gibson (1975) noted phosphatase pro- far apart as Windermere and Lake Michigan, that duction in a freshwater Synechococcus at external vernal ‘blooms’ of planktic diatoms, featuring sig- concentrations of <4 µMP. nificant increments in chlorophyll concentration Eukaryotic phytoplankton has not been inves- and a ≥30-fold increase in the concentrations of tigated to this level of biochemical detail. How- cells in suspension take place against only small ever, it seems likely that analogous mecha- changes in MRP concentration. As revealed by nisms and similar sensitivities apply among the conventional chemical analyses, these scarcely many phytoplankters that inhabit aquatic envi- exceed 0.1 µM(i.e.∼3mgPm−3:Reynolds, ronments in which phosphate concentrations are 1992a). Some planktic algae and bacteria, at least, frequently <1 µMPand, often, an order of mag- are sufficiently well adapted to gather phospho- nitude less again (<0.1 µMP,i.e. <10−7 mol L−1, rustofund several cell doublings despite chron- <3 µgPL−1). ically low ambient MRP concentrations. Most of our present knowledge of the phosphorus-uptake kinetics of phytoplankton 4.3.2 MRP-uptake kinetics comes from the numerous laboratory studies on Phosphorus uptake and transport in microorgan- named species, carried out mainly in the mid- isms are thought to depend on two separate dle years of the last century. Some of these uptake mechanisms. In the Enterobacteria, such have been used in the compilation of compen- as Escherichia coli, which can normally experi- dia and reviews (Reynolds, 1988a, 1993a;Padisak,´ ence a much higher external concentration than 2003). In order to make valid interspecific com- afree-living phytoplankter, a low-affinity mem- parisons (such as those in Fig. 4.5), it is nec- brane transport system normally operates (Rao essary to convert often disparate measurements and Torriani, 1990). If external phosphorus con- to appropriate common scales. Only volume- or centration falls, however, to ≤20 µM(∼0.6 mg P carbon-specific uptake rates of planktic cells lend l−1), the second, high-affinity system is activated. themselves to some generalisations. One of these This one is ATP-driven and is linked directly is that the maximum phosphorus-uptake rates to periplasmic phosphate-binding sites. Working (VUmax )ofarangeoffreshwaterphytoplankton with a cultured strain of the marine cyanobac- are comparable, at least within 2 orders of mag- terium, Synechococcus sp. WH7803, Scanlan et al. nitude, when expressed per unit area of algal (1993)demonstrated the accelerated synthesis of unit surface (Fig. 4.5b: 0.5 to 35 × 10−19 mol P several intracellular polypeptides as their cul- µm−2 s−1). When normalised to cell carbon, the tures became increasingly depleted of soluble same data translate to maximum uptake rates 156 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

Figure 4.5 (a) Absolute maximal phosphorus uptake rates too concerned about phosphorus-limited uptake of phytoplankton cells and colonies as reported in the ratesthat remain capable of saturating growth literature reviewed by Reynolds (1988a) and expressed on a rates down to external concentrations (reading common scale. (b) The same data normalised to the surface from Fig. 4.4)oftheorder of 0.1 × 10−6 mol P L−1 areas of the cells or colonies as appropriate. (c) The same (see also Section 5.4.4). data normalised to cell carbon (the shaded part of the Nevertheless, ambient concentrations of MRP histograms correspond to the fastest carbon-specific rate of in some natural waters may be chronically con- P assimilation in growth; the balance represents spare strained to this order and, in many others, be fre- capacity (note the logarithmic scales). The algae are Ana, Anabaena flos-aquae; Ast, Asterionella formosa; Chla, quently drawn down to such levels. We may read- Chlamydomonas sp.; Chlo, Chlorella; Din, Dinobryon divergens; ily accept that phytoplankton tolerant of such Eud, Eudorina unicocca; Mic, Microcystis aeruginosa; Per, conditions must invoke high-affinity mechanisms Peridinium cinctum; Plaa, Planktothrix agardhii; Scq, Scenedesmus forphosphorus uptake. Our interest should be quadricauda: Vol, Volvox aureus. Data presented in Reynolds sharply focused on the shape of the uptake curve (1993a) and redrawn from Reynolds (1997a) with permission. at the extreme left-hand side of Fig. 4.4 and the beneficial distortion represented by a relatively low half-saturation concentration (KU). Indeed, of between 0.1 and 21 × 10−6 mol P (mol cell thelower is the concentration required to half- C)−1 s−1.Againstthetheoretical requirement for saturate the uptake of phosphorus, then the phosphorus to sustain a doubling of the cell car- greater isthelikely ability of the alga to fulfil bon (9.4 × 10−3 mol P (mol cell C)−1), these max- its requirements at chronically low external con-

imal P-uptake rates (VUmax )wouldbesufﬁcient centrations. The faster is the uptake capacity at to meet the growth demand in from 440 to 94 thelow,markedly sub-saturating resource levels, 000s(∼7minutes to 26 h), supposing a saturat- then the greater is the alga’s afﬁnity for phospho- ing concentration and a constant rate of uptake. rus and the greater is its ability to compete for The steady-state phosphorus requirements of the scarce resources. same planktic species growing at their respec- Pursuing this reasoning further, Sommer’s tive maximal cellular growth rates (from Chap- (1984)experiments distinguished several differ- ter 5)areinserted in Fig. 4.5ctoemphasise a ing adaptive strategies among freshwater phyto- second generalisation. It is that we need not be plankton for contending with variable supplies of PHOSPHORUS 157

∼ ◦ Ta b l e 4.2 Some species-speciﬁc values of maximum phosphorus uptake rate (VUmax )at 20 C and the external concentration of MRP required to half-saturate the uptake rate (KU, being the concentration required

to sustain 0.5 VUmax )

−1 a Species VUmax µmol P KU µmolPL References (mol cell C)−1 s−1 Chlamydomonas reinhardtii 7.35 0.59 Kennedy and Sandgren (unpublished, quoted by Reynolds, 1988a, with permission) Chlorella pyrenoidosa 25.12 0.68 Nyholm (1977) Asterionella formosa 0.51 1.9–2.8 Tilman and Kilham (1976) Dinobryon sociale 0.21 0.39 Lehman (1976) Scenedesmus quadricauda 3.4 1.2–4.0 Nalewajko and Lean (1978) Anabaena ﬂos-aquae 10.5 1.8–2.5 Nalewajko and Lean (1978) Peridinium sp. 0.11 6.3 Lehman (1976) Eudorina elegans 0.34 0.53 Kennedy and Sandgren (unpublished, quoted by Reynolds, 1988a, with permission) Planktothrix agardhii 5.41 0.2–0.3 van Liere (1979), Ahlgren (1977, 1978) Volvox aureus 5.24 1.62 Kennedy and Sandgren (unpublished, quoted by Reynolds, 1988a, with permission) Microcystis aeruginosa 1.95 0.3 Holm and Armstrong (1981)

a The original data come from the works cited, as recalculated to a common scale of cell-carbon speciﬁcity by Reynolds (1988a).

phosphorus. Species might be relatively velocity- interexperimental variability, even for the same adapted,inwhichhigh rates of cellular growth species. The values noted in Table 4.2 are those and replication (r )arematchedbysuitablyrapid used in the construction of Fig. 4.5.Toanextent, rates ofnutrient uptake (VUmax ), or else, they may VUmax is necessarily greater than the rate of be more storage-adapted,inwhichrapid, oppor- deployment of phosphorus in new cell mate- tunistic uptake rates exceed relatively slow rates rial, supposing that this corresponds to rmax (at of deployment in growth, thereby permitting a 20 ◦C) and that the cell quota remains con- net accumulation of an intracellular reserve of stant. From this, it may also be deduced that phosphorus. These adaptations are said to be dis- the uptakerate, VU, has to be markedly under- tinguished by differences in the species-specific saturated for a considerable time before r can / ratio (VUmax rmax). Species may also show a ten- be said to be P-limited. The most helpful adap- dency tobemoreorlessaffinity-adapted accord- tation to enable algae to deal with chronically / ing to the species-specific ratio, VUmax KU;assug- low external MRP concentrations is a very low gested, high affinity is imparted by a low KU half-saturation coefficient. However, it is clearly requirement. relevant for such algae to be able still to func- Sommer’s terminology is helpful but the tion on a relatively low internal phosphorus derived measures are themselves subject to quota. Davies’ (1997)recentinvestigations of the 158 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

cell-phosphorus-related growth kinetics of nat- In another line of investigation, it has been ural Asterionella populations during the spring- shown that some strains of Cyanobacteria are bloom period in the English Lakes are illus- able to maintain full growth down to exter- trative. Plotting cell-increase rates against the nal concentrations of 100 nmol P L−1 (∼3 µg corresponding cell P quotas at the time of their L−1), without producing any of the regulator pro- sampling, Davies (1997)wasable to fit a sin- teins that signal the activity state of the trans- gle, statistically significant Michalis–Menten-type port system to the controlling operons (Mann, curve, that suggested growth rate was fully sat- 1995; Scanlan and Wilson, 1999). As suggested urated by cell quotas of 5–10 pg P (cell)−1 (or, in Section 4.2.2,thepresence of regulator pro- roughly, 0.023–0.045 mol cell P (mol cell C)−1) teins is indicative of incipient cell starvation, and half-saturated at about 0.7 pg P (cell)−1 (i.e. triggering the appropriate intracellular defensive ∼0.003 mol cell P (mol cell C)−1). Plotting cell reactions. Work on the bacterium Vibrio (Kjelle- phosphorus as a function of the MRP concentra- berg et al., 1993) showed that symptoms include tion in the lake water at the time of collection, asharp slowdown in cell growth, following an she showed that maintenance of a quota of this abrupt deceleration in the rates of protein syn- magnitude was possible at an external concen- thesis. Assembly of macromolecules is halted by tration of round 0.75 µgPL−1 (0.024 µmol P the action of synthesis inhibitors, followed by the L−1). Plainly then, good growth is still possible reorganisation of the cell components and the in the face of external depletion so long as the adjustment of the fatty-acid content of the mem- cell quota is maintained. In contrast, at the very branes to resist lysis. In turn, these actions are minimum cell quota (e.g. of Mackereth, 1953) cor- followed by a decline in the rate of respiration responding to ∼0.0003 mol cell P (mol cell C)−1, and other metabolic activity. growth is quite impossible. Central to these reactions are the transduc- ing signals. Certain nucleotides are known to increase in response to falling nitrogen concen- 4.3.3 Metabolic-rate limitation by tration and amino-acid synthesis. One of these, phosphorus guanosine 3,5-bipyrophosphate (ppGpp), is gen- How cells function in the face of low internal P erated in nitrogen-starved E. coli (Gentry et al., resources and very low external P supplies has 1993)andVibrio (Kjelleberg et al., 1993). Homo- been investigated in recent years, using a vari- logues to these are found in cyanobacterial cells ety of alternative techniques that overcome the experiencing a sharp reduction in photon flux problem of how to quantify chemically the small (Mann, 1995). Incipient starvation and ribosomal amounts of determinand present. For instance, stalling are thought to lead to ppGpp synthe- Falkner et al. (1989)applied force-flow functions, sis and, thence, to the communication of star- derived by Thellier (1970), to demonstrate that vation. Mann’s group was able to grow plank- thetypical external concentrations of phosphate tic cyanobacteria in media in which phosphorus below which cells of Cyanobacteria fail to balance concentrations fell to <0.1 µM(i.e. less than 3 µg their minimal maintenance requirements indeed PL−1) before compounds like ppGpp began to fall within the range 1–50 nmol L−1 (0.03–1.5 µg appear in the cells. This is strongly suggestive PL−1). In the application of Aubriot et al. (2000), of the probability that cells do not experience the importance of the affinity of uptake mecha- phosphorus shortages in media containing MRP nisms and of the opportunism to invoke them in concentrations greater than this. the face of erratic supplies was especially empha- Finally, in this context, the emerging tech- sised. Hudson et al. (2000)applied a radiobioas- nique of using fluorimetric labelling to detect say technique which was also able to demonstrate theintracellular transients induced by incipient that the amount of phosphorus in the medium nutrient starvation (the so-called NIFT, nutrient- supporting active phytoplankton populations can induced fluorescent transients) has been applied fall less than 10 nmol L−1 (i.e. <10−8 M), without to microalgae grown under P-replete and P- necessarily impairing productivity. deficient conditions to identify the reactivity PHOSPHORUS 159 of the cells. According to the experiments of those photosynthetic organisms capable of Beardall et al. (2001), NIFT responses were wholly supplementing or, perhaps, fulfilling their lacking in eachoffourspeciesoffreshwa- requirements for nutrients and carbon by ingest- ter microalgae in media containing ≥0.13 µM ing organic particulates are called mixotrophs. (4 µgPL−1). The best-known examples come from among the These various threads lead to a strong consen- dinoflagellates (marine and freshwater Gymno- sus that phosphorus availability does not limit diniales and Gonyaulacales) and from among phytoplankton activity and growth before the theChromulinales, including Ochromonas (Rie- MRP concentration in the medium falls almost mann et al., 1995;Geider and MacIntyre, 2002). to the limits of conventional analytical detec- Certain pigmented cryptomonads are reputedly tion. At this point, phytoplankton may draw on mixotrophic (Porter et al., 1985): this need not be internal reserves such that activity is not imme- surprising insofar as the phagotrophic abilities diately suppressed by lower external concentra- of the typically colourless cryptomonad genera tions. Even at <0.1 µM, it is not the concentra- (such as KatablepharisandCyathomonas)havelong tion of phosphorus that is critical so much as the been recognised (Klaveness, 1988). As a source of capacity of the intracellular storage and the affin- phosphorus, bacterivory and phagotrophy offer ity of the biological uptake mechanism for the arich alternative to scarce dissolved inorganic small amounts of bioavailable phosphorus being sources and, unlike phosphatase secretion, turned over in the system (Hudson et al., 2000). theavailable resource would seem to be less Two other mechanisms for contending with restricted. However, a low-phosphorus environ- MRP limitation of metabolic activity are avail- ment pervades all its trophic levels: bacterivory able to certain species of phytoplankton. The first is not a sustainable alternative to deficient MRP involves the production of extracellular phos- if the bacteria are themselves simultaneously P- phatases. Many freshwater species, in fact, pro- limited. Mixotrophy is particularly beneficial as a duce alkaline phosphatases which liberate phos- supplementary source of nutrient in those (gen- phate from organic solutes that can then be erally smaller) water bodies that receive inputs absorbed by the alga (Cembella et al., 1984). They of terrestrial organic matter) but are otherwise are produced in response to external MRP defi- quite oligotrophic (Riemann et al., 1995). ciency, almost as soon as it develops (Healey, 1973). In the past, phosphatase activity has been 4.3.4 Capacity limitation and potential considered to be indicative of phosphorus limita- phosphorus yield tion (Rhee, 1973). There is little doubting the fact While it is clear that (probably all) phytoplank- that phosphorus thus sequestered increases the ton can take up and assimilate the entire mea- resource availability to the cell. For phosphatase surable MRP resource base, without first experi- production to be able to offer any survival advan- encing rate limitation, and that, thereafter, some tage, however, the phosphatase must be retained species at least are extremely effective in main- at or close to the cell surface (Turpin, 1988). Phos- taining their biomass, it is no less clear that phatase activity might then raise significantly the themaximum supportable biomass, Bmax, cannot ability of algae to tolerate chronically P-deficient exceed the capacity of the most scarce resource conditions. There is little evidence to suggest that relative to demand (Box 4.1). It remains generally phosphatase production does much to enhance true that, in a large number of larger, deeper the growth dynamics ofassemblages, or any lakes in the higher latitudes, phosphorus is the component species, when inorganic phosphorus nutrient that is exhausted first and, thus, the one sources are effectively exhausted (Reynolds, that imposes the upper limit on the supportive 1992a). capacity of the location. The generality is sup- The second mechanism involves the ported by the well-known ‘Vollenweider model’ phagotrophic ingestion of organic particles, and the impressive fit of the average phytoplank- including especially other organisms such as ton biomass present in a selection lakes to the bacteria. As indicated earlier (Section 3.4.4), corresponding average phosphorus availability in 160 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

the samelakes(Vollenweider, 1968; 1976;Organ- known resource availability. This same regression isation for Economic Co-operation and Develop- equation (4.13) has been shown to be applicable ment, 1982;seealso Section 8.3.1). Several generi- to theprediction of the maximum algal concen- cally similar regression models from the same era tration in other British lakes in which the MRP (Sakamoto, 1966;Dillon and Rigler, 1974;Oglesby falls to analytically undetectable levels (Reynolds, and Schaffner, 1975)provide analogous findings. 1992a;Reynoldsand Davies, 2001), enhancing the It has to be recognised that the datasets are supposition that the resource-limited yield is predominated by information from just the well- dictable from the available resource. It has also studied, northern-hemisphere oligotrophic lakes been used to estimate the chlorophyll-carrying in which later understanding confirms the max- capacity of the MRP resource in lakes where the imum phytoplankton carrying capacity is deter- maximum crop is susceptible to other limita- mined by the availability of phosphorus. It has tions (Reynolds and Bellinger, 1992)andisnow equally to be recognised that the condition does incorporated into the capacity-solving model of not apply everywhere – itislesslikelytoapply Reynolds and Maberly (2002). to large, continental lakes at low latitudes, espe- Whereas, it was originally estimated that: cially to lakes in arid regions, and to smaller, log[chla] = 0.585 log[MRP] + 0.801 shallower lakes at all latitudes. It certainly does max max not apply to the open oceans, although its rele- (4.14) vance to coastal waters should not be dismissed. where [MRP]max is the highest observed concen- Nevertheless, there remains a danger in suppos- tration of MRP and [chla]max is the predicted ing that the Vollenweider-type equations can be maximum chlorophyll (both units in µgl−1 or used to predict phytoplankton biomass in a given mg m−3), the later applications are used to pre- individual lake. Plainly, the criterion of capacity dict an instantaneous yield against the supposed limitation by phosphorus must be demonstrable. bioavailability of P. Thus, Moreover, the equations are statistical and not . [chla] = 6.32[BAP]0 585 (4.15) predictive, indicating no more than an order-of- max magnitude probability of average biomass that Estimating exactly what is bioavailable, without may be supported. The trite circumsciption of enormous analytical effort, remains problematic. lakes or seas as being ‘phosphorus-limited’ (or However, on the assumption that phosphatase ‘nitrogen’, or‘anything else’ limited’) is to be activity will raise the supportive capacity only avoided completely. negligibly and that mixotrophic enhancement Several authors have tried to express the max- rarely applies outside the habitats in which it is imum yield of biomass as a function of nutrient recognised (see Section 4.3.3), then the resource availability (Lund, 1978;Reynolds, 1978c). Lund currently available to the phytoplankton is rep- regressed maximum summer chlorophyll against resented by the unused MRP in solution plus total phosphorus in a small lake (Blelham Tarn, theintracellular phosphorus already in the algae. UK) in each of 23 consecutive years during which The minimum estimate of the resource in intra- thelake underwent considerable eutrophication. cellular store can be gauged simply by reversing Reynolds (1978c)chosetoregress the chloro- Eq. (4.15)tosolvetheBAPinvestedinthestanding phyll concentrations measured in several con- crop. trasted lakes in north-west England at the times [cell P] = (0.158[chla])1.709 (4.16) of their vernal maxima against the correspond- min ing MRP concentrations at the start of the spring BAP can be estimated by first solving Eq. (4.16), growth. Despite certain obvious drawbacks to based on the existing chlorophyll concentration, this approach (no allowance was made for inter- then adding the equivalent intracellular cell P mediate hydraulic exchange and nutrient supply, content thus predicted to the existing MRP con- neither were any other loss processes computed), centration. Substituting this solution in Eq. (4.15) the regression comes close to expressing the gives an instantaneous carrying capacity and notion of a direct yield of algal chlorophyll for a potential chlorophyll yield. NITROGEN 161

L−1 (i.e. 6.32 µgchla (µgBAP)−1); 10 µgBAPL−1 will support ≤24 µgchla L−1 (i.e. 2.4 µgchla (µgBAP)−1), whereas the return on 100 µgBAP L−1 is ≤91.4 µgchla L−1 (i.e. 0.91 µgchla (µg BAP)−1). A small, biomass-limiting BAP has to be used very efficiently but a larger base, one that perhaps challenges the next potential capacity of the biomass, is used with more ‘luxury’, at least before the external resource is exhausted. In terms of biomass, the effect may be even more striking, bearing in mind the tendency towards relatively lower biomass-specific chlorophyll contents of phytoplankters in sparse, light-saturated, nutrient-limited populations. Supposing a constant quota of 0.02 µgchla (µgcellC)−1 (see Section 1.5.4), the phytoplankton carbon yields available from 1–100 µgBAPL−1 may be calculated to be from 316 down to 45.7 µgC(µg BAP)−1. The corresponding range of phosphorus quotas, 0.0012–0.0085 mol P (mol cell C)−1,neatly spans the condition of cells close to their minimum (q0)tobeingclose to the Redfield ideal (C : P ratio >800 to 118). This outcome is possibly more realistic than the direct solution of Bmax = Ki/q0 (as proposed in Box 4.1), which may greatly exaggerate outcomes extrapolated from abundant resource bases.

Figure 4.6 (a) Observed maximum chlorophyll 4.4 Nitrogen: requirements, concentrations in lakes in north-west England as a function of bioavailable phosphorus, as detected by Reynolds (1992a) and sources, uptake and the regression originally proposed by Reynolds (1978c)on metabolism in phytoplankton the basis of a study of just three lakes (see Eqs. 4.14, 4.15). (b) A later, larger dataset of observed chlorophyll maxima from UK lakes plotted against the predtion of the Reynolds Nitrogen is the second element whose relative regression. As expected, a majority of points lie below the scarcity impinges upon the ecology of phyto- predicted maximum but a number are above it, sometimes plankton. As a constituent of amino acids and, substantially so. Graphs redrawn from Reynolds and Davies thus, all the proteins from which they are syn- (2001) and Reynolds and Maberly (2002). thesised, nitrogen accounts for not less than 3% of the ash-free dry mass of living cells (about 0.05 molN(molC)−1). This rises to around 7–8.5% in Besides being broadly veriﬁable from observa- replete cells, capable of attaining rapid growth tions (see Fig. 4.6b), Eq. (4.15)isconsistent with (0.12–0.15 mol N (mol C)−1,i.e. 6.6–8.2 C : N) (see the underpinning physiology. The slope of the also Section 1.5.3), and to 10–12% in cells stor- equation as plotted in Fig. 4.6apredicts a higher ing condensed proteins. However, molecular C : N return in chlorophyll for the BAP invested at low ratios of <6invegetative cells are usually con- availabilities. Thus, 1 µgBAPL−1 is predicted strued to be symptomatic of carbon deprivation to be capable of supporting up to 6.32 µgchla (see Section 3.5.4). Relative to cell phosphorus, 162 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

the nitrogen content of replete cells is generally extreme, temperate shelf waters, especially those in the range 13–19 mol N (mol P)−1;highermolec- influenced by large fluvial outfalls, may have ular ratios (>30 N : P) are indicative of intracellu- nitrate levels of 60–70 µM. In lakes and rivers, lar phosphorus deficiency; lower ratios (<10 N : P) especially in the temperate regions, the nitrate are consistent with nitrogen shortages. availability may reach 50–65 µMinlate winter (generally the time of minimum biological demand, slowest terrestrial denitrification and 4.4.1 The sources and availability of maximum leaching: George, 2002). In regions nitrogen to phytoplankton subject to intensive modern agriculture and rel- Despite the abundance of the element in the atively heavy applications of nitrogen fertiliser, atmosphere, relative inertness of nitrogen gas leachate may raise the dissolved inorganic nitro- rather restricts most photautotrophic exploita- gen concentration in receiving river waters to up tion to nitrogen compounds. The element is also to1mM(14gNm−3). However, on the ancient poorly represented in the Earth’s crust: its occur- continents at lower latitudes and, especially, in rence is largely restricted to biogenic layers in arid regions, the amount of nitrate lost from sedimentary rocks. The principal forms of com- catchment topsoils is usually small and subject bined nitrogen available to photoautotrophs are to further microbial denitrification. Thus, receiv- − the ions nitrate, nitrite and ammonium (NO3 , ing waters tend to be relatively more deficient in − + −3 NO2 and NH4 ), although this may not be exclu- nitrate (1–10 µM, 15–150 mg N m )than in phos- sively true for all phytoplankton (see below). Very phorus (Reynolds, 1997a). Even at temperate lat- little of the available resource, either in lakes itudes, however, barren upland catchments may or in the sea, is due to direct atmosphere-to- be capable of delivering only low concentrations water linkages: most of the sources of combined of nitrate (≤15 µM). There is considerable evi- nitrogen in water are imported from terrestrial dence (Soto et al., 1994; Diaz and Pedrozo, 1996) systems or are recycled within the aquatic sys- of a nitrogen-regulated carrying capacity in the tem. The ready solubility of most inorganic nitro- oligotrophic lakes of Patagonia and the southern gen compounds, the rarity of their occurrence Andes (total N <300 µgNL−1, some <100 µg in secondary polymers and the redox sensitivity NL−1;equivalent to 7–20 µMasnitrate supplied). of their ionic configurations assist the frequency These observations prompt questions about com- of transformations and relocation. The biogeo- parative current deliveries of nitrate in northern- chemical cycling of nitrogen is mediated mainly hemisphere rainfall, which may have been rela- by organisms. Accordingly, its turnover is regu- tively more augmented by industrial airfill than lated predominantly at the physiological level, in the southern hemisphere. and so is extremely rapid when compared to the Nitrate ions are sensitive to the low-redox cycling of other elements such as phosphorus or conditions (<+300 mV) in sediments, the deep silicon. waterofstratified, eutrophic lakes and seas and Of the three main sources of inorganic com- in other (usually polluted) waters experiencing bined nitrogen, it is the highest-oxide form that high biochemical oxygen demand. Reduction to occurs most widely in solution in lakes and seas. lower oxides (nitrite), to nitrogen gas and ammo- In the deep oceans, nitrate concentrations are nia is accelerated through microbial oxidation of generally in the range 20–40 µM (280–560 mg organic carbon and its requirement for alterna- Nm−3)but, towards the surface (the upper tive electron acceptors to the diminishing quan- 50–100 m or so), they may be drawn down tities of oxygen. Specifically, the activites of the severely as a result of algal and microbial uptake, denitrifying nitrate reducers like Thiobacillus deni- to levels close to the limits of conventional anal- trificans and various pseudomonad bacteria result ysis (∼1 µM). Among the most nitrate-deficient in the venting of nitrogen gas to the atmo- waters are those of the North Pacific Gyre, the sphere. Nitrate ammonification occurs through subtropical Atlantic (including the Sargasso) and theagency of facultatively anaerobic bacteria, Indian Oceans (McCarthy, 1980). At the other such as Aeromonas, Bacillus, Flavobacterium and NITROGEN 163

Vibrio,first reducing nitrate to nitrite. This may DON pool as well as benefit from the microbial be excreted or, under appropriate conditions, liberation of DIN. some of these organisms reduce the nitrite further, to hydroxylamine (NH2OH) and ammonium 4.4.2 Uptake of DIN by phytoplankton (Atlas and Bartha, 1993). Phytoplankton are generally capable of active The ammonium ions are more soluble (so less uptake of DIN from external concentrations as volatile) than nitrogen, hence the reduction is low as 3–4 mg N m−3 (0.2–0.3 µM). Although more of a transformation within the pool of inor- nitrate is usually the most abundant of the DIN ganic nitrogen, denoted by DIN (dissolved inor- sources in the surface waters of lakes and seas, ganic N), rather than a loss therefrom. Whereas ammonium is taken up preferentially if concen- nitrate may dominate the DIN fraction in the trations exceed some 0.15–0.5 µMN(2–7 mg open water of seas and lakes, in-situ biologically Nm−3). This is because the initial intracellu- mediated redox transformations may lead to the lar of assimilation of nitrogen proceeds via a accumulation of comparable quantities of nitrite reductive amination, forming glutamate, and a and, especially, ammonium (to >1gNm−3, subsequent transamination to form other amino 70 µM) in microaerophilous or anoxic environ- acids. The substrate is apparently always ammo- ments. Ammonium is typically also present in nium (Owens and Esaias, 1976). Thus, it is both oxic, unpolluted surface waters, though rarely in probable and energetically preferable that the excess of ∼150 mgNm−3 (or ≤10 µM) (Reynolds, alga should use ammonium directly; nitrate and 1984a). nitrite have to be reduced prior to assimilation in The sources of nitrogen available to phyto- reactions catalysed by (respectively) nitrate reduc- plankton may be supplemented by certain dis- tase and nitrite reductase, so adding to the ener- solved and bioavailable organic nitrogen com- getic cost of nitrogen metabolism. This differ- pounds (DON). These include urea (McCarthy, ence in the energy requirement for the assim- 1972), which is produced mainly as an excretory ilation of nitrate and ammonium is reflected in metabolite of animal protein metabolism, as well thephotosynthetic quotient, being about 1.1 mol −1 as through the bacterial degradation of purines O2 (mol CO2) when ammonium is assimilated and pyrimidines. McCarthy’s (1980) compilation and 1.4 when nitrate is the substrate (Geider and of urea concentrations recorded in the litera- McIntyre, 2002,quoting Laws, 1991). Eppley et ture reveals concentrations under 3 µg-atoms al. (1969a)devised an assay for nitrate-reductase NL−1 (≤3 µMN)intheseaandupto∼9 µM activity in natural populations and which shows, in some North American rivers. Other sources consistently, that it is suppressed by ammonia of organic nitrogen directly available to phyto- concentrations exceeding 0.5–1.0 µg-atoms N L−1 plankton include the small amounts (generally (0.5–1.0 µMN)(see also McCarthy et al., 1975). <1 µMN)offreeaminoacidpresent in lakes More recently, the genes encoding the kinases and seas (McCarthy, 1980). The relevant deam- forbacterial nitrogen transport have been recog- inases are said to be produced by microalgae nised (Stock et al., 1989)and the action of ammo- only under conditions of DIN deficiency (Saubert, nium in suppressing them has been similarly 1957;Turpin, 1988). demonstrated (Vega-Palas et al., 1992). Of course, the size and dynamics of the DON The kinetics of DIN uptake by marine phy- pool is of additional indirect relevance to the toplankton have been studied extensively; those pelagic function. Far from being refractory, DON of freshwater species having received relatively is frequently the major source of nitrogen avail- less attention. Half-saturation concentrations for able to planktic microbes (>80% of the nitrogen uptake (KU)bynamed, small-celled oceanic available in oceanic surface waters is organic: species in culture (Eppley et al., 1969b; Caperon Antia et al., 1991)and some of it is evidently and Meyer, 1972;Parsons and Takahashi, 1973) metabolised rapidly (in days rather than weeks; fall within the range 0.1–0.7 µMN(when see the review of Berman and Bronk, 2003). Plank- nitrate is the substrate) and 0.1–0.5 µMN tic algae and cyanobacteria may contribute to the (with ammonium). Among neritic diatoms, the 164 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

corresponding ranges are 0.4–5.1 µMNO3.N and associated with prokaryotes. This ability to ‘fix’ 0.5–9.3 µMNH4.N. Some half-saturation con- (reduce) elemental dinitrogen to ammonia is a centrations for nitrate uptake among freshwa- widespread trait among obligate heterotrophic terplankters are available (Lehman et al., 1975; chemolithotrophic bacteria, the photosynthetic Reynolds, 1987a; Sommer, 1994), typically falling bacteria and the Cyanobacteria. Certain of the in the range 0.3–3.0 µMN.Themaximum rates latter, most especially, some of the nostocalean of DIN uptake at 20 ◦C (calculated to be generally genera, are the only members of phytoplankton equivalent to 0.6 to 35 µmol N (molcellC)−1 s− 1) to have this capacity. Nitrogen fixation may have are competent to saturate growth demand (D/S been a crucial step in the evolution of autotrophy < 0.1 to 0.2: Riebesell and Wolf-Gladrow, 2002). in an increasingly oxygenic atmosphere, because As in the general case (see Section 4.2.3), uptake of the relative volatility and extreme sparseness and consumption achieve parity at steady rates of of nitrogen in the lithosphere. Ammonia was also growth, at external DIN concentrations generally rare owing to its photolysis in an atmosphere ≤7 µmol N L−1. relatively undefended against ultraviolet radia- Conversely, nitrogen availability is unlikely tion. The early emergence of biological fixation, to constrain phytoplankton activity and growth through the production of the dinitrogen reduc- before the DIN concentration in the medium falls tase enzyme, provided the first means of entry to below 7 µmol N L−1 (∼100 mgNm−3)in into ecosystems of large quantities of combined the case of large, low-affinity species or below nitrogen (Falkowski, 2002). The enzyme catalyses ∼0.7 µmol N L−1 (∼10 mg N m−3)inthecase of thereduction of dinitrogen to ammonium using oceanic picoplankton). Activities become severely reductant produced via carbohydrate oxidation. constrained once the cell nitrogen content falls Nitrogen fixation is a respiratory reaction: −1 below ∼0.07 mol N (mol C) , when the cell reacts + 2N + 4H+ + 3[CH O] + 3H O6 4NH + 3CO to its internal N deficiency by closing down non- 2 2 2 4 2 essential processes. The minimum cell quota (q0) (4.17) of nitrogen in phytoplankton cells is said to be Interestingly, dinitrogen reductases are based on 0.02–0.05 mol N (mol C)−1 (Sommer, 1994). iron–sulphur prosthetic groups that are redox Applying the statistic (K/q0), the ultimate sensitive: the enzymes operate only under strictly yield or carrying capacity of the available inor- anaerobic conditions (as they did when they ganic combined nitrogen isaround20molC evolved). Nitrogen fixation is rapidly inactivated (mol N)−1,withapossible extreme of ∼50 (17– in the presence ofoxygen(Yates,1977). In order 42gC:gN).Beforetheinternalnitrogen to fix nitrogen in an oxic ocean, the enzyme must becomes yield limiting, however, the equivalence be protected from poisoning by oxygen. As Paerl is not likely to much exceed 10 and perhaps as (1988)remarked, for compatibility between oxy- little as 5 mol C (mol N)−1 (say, 8.5 to 4.2 g C : g genic photosynthesis and anoxic nitrogen fixa- N). In terms of chlorophyll yield, the supportive tion to have developed represents a remarkable capacity of 5–20 mol C (mol N)−1 is equivalent evolutionary achievement for the Cyanobacteria. to some 0.08–0.34 g chla :gN.Thefactor used Until the 1960s, the nitrogen-fixing capability in the capacity-solving model of Reynolds and of Cyanobacteria had only been suspected from Maberly (2002), which is biassed by data from sys- nitrogen budgets (e.g. Dugdale et al., 1959). The tems that are more likely to be P-deficient, is 0.11 introduction of the acetylene-reduction assay for gchla :g N. nitrogenase activity (Stewart et al., 1967)made it possible to investigate which species fixed nitro- 4.4.3 Nitrogen fixation gen, under what conditions and at which loca- The ability to exploit the atmospheric reservoir of tions. Among the freshwater Nostocales, fixation nitrogen gas (or, at least, that fraction dissolved is confined to the heterocysts (sometimes called in water: at sea-level air-equilibrium, ∼20 mg heterocytes). These are specialised cells differenti- nitrogen L−1 at 0 ◦C, falling to ∼11 mg L−1 ated at intervals along the vegetative filaments at 20 ◦C) as a source of nutrient is exclusively (Fay et al., 1968). Their thick walls defend the NITROGEN 165 intracellular anaerobic conditions necessary for trations has been demonstrated in the laboratory theenzyme function. They are differentiated in (Ohmori and Hattori, 1974;seealsoKerbyet al., life from normal vegetative cells responding to 1987), albeit at higher levels. On the other hand, nitrogen deficiency. Besides the thickening of theisolates of non-nitrogen-fixing Cyanobacteria thewall, the cells lose their blue-coloured phy- from nitrogen-deficient lakes (Merismopedia, Micro- cocyanin. However, they retain a chlorophyll- cystis, Synechococcus)usedintheexperiments of based light-harvesting capacity, attached to a Blomqvist et al. (1994), all responded much more functional PS I and ferredoxin transfer pathway positively to ammonium enrichment than they to NADP reduction (cf. Section 3.2.1)butthe did to nitrate additions. They also responded less oxygen-evolving PS II is, of course, defunct (Wolk, positively to nitrate additions than did plank- 1982;Paerl, 1988). tic eukaryotes, including a Peridinium. Bearing in Heterocysts are not permanent features. Natu- mind that the group evolved in an ammonium- ral populations of Anabaena, Aphanizomemon,etc. scarce, nitrate-free, anoxic environment, a high can increase to significant levels of biomass with- affinity for ammonium nitrogen and a low-redox out producing heterocysts. Differentiation is a mechanism for its intracellular enhancement facultative response to falling external DIN con- would appear to be useful adaptations. Both centrations, to the extent that their relative fre- retain a relevance to survival and relative suc- quency (heterocysts : vegetative cells) has been cess of distinctive members of the group in mod- taken by ecologists to be a sign of incipient ern environments that are extremely nitrogen- nitrogen limitation (Horne and Commins, 1987; deficient or where relatively high phosphorus Reynolds, 1987a). Their induction and distribu- levels drive biomass accumulation of production are regulated genetically by DNA promoters ers able to exploit extraneous sources of (see Mann, 1995,fordetails). Most of the rele- nitrogen. vant observations on their production (reviewed Besides low external DIN concentrations and in Reynolds, 1987a)reportthe incidence of alow-redox, microaerophilous proximal environ- increased heterocyst frequency, from <1:10000 ment, adequate nitrogen fixation remains depen- vegetative cells to as high as 1 : 10, in popula- dent upon high electron transport energy as tions of Anabaena, Aphanizomenon and Nodularia, well as high rates of endogenous respiration coincident with DIN concentrations falling below (Paerl, 1988), driven (in this instance) by photo- 300–350 mg m−3 (19–25 µM). The higher ratios synthesis and good insolation. The low reactiv- are noted particularly at DIN concentrations ≤80 ity ofN2 requires that large amounts of ATP and mg m−3 (≤6 µM N). Given that these concentra- reducing power are invested in the nitrogenase tions will, ostensibly, at least half-saturate the reaction (Postgate, 1987). Nitrogen fixation also maximum rates of uptake of combined nitrogen requires phosphorus: Stewart and Alexander and completely saturate nitrogen demand (see (1971) showed that nitrogenase activity was above), the sensitivity of heterocyst production steadily lost in cultures of heterocystous Anabaena to rather higher DIN concentrations is puzzling. and other nostocalean species transferred to P- One possible explanation is that the heterocyst free medium and was not restored without the production and, indeed, the nitrogenase activ- addition of phosphate to the medium to a con- ity that they accommodate are actually sensitive centration equivalent to 5 mg P m−3 (∼0.16 µM to the external concentrations of ammonium, P). The availability of molybdenum and/or vana- which may represent much the smaller fraction dium/iron for the core of the nitrogenase enzyme of the total DIN pool and is also the one that is is biochemically essential to nitrogen fixation the more rapidly drawn down. This would also (Postgate, 1987; Rueter and Petersen, 1987). It have to imply that the nitrogen-fixation response cannot be assumed that low ambient nitrogen is a preferential reaction to low external levels of levels are automatically compensated by nitro- −3 NH4.N (<0.5 µMN,or<7mgNm )andnotof genfixation and the successful exploitation of nitrate. Direct sensitivity of nitrogenase produc- such conditions by N2-fixing Cyanobacteria, with- tion in Anabaena flos-aquae to ammonium concen- out demonstrable satisfaction of the constraints 166 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

imposed by light, phosphorus and micronutrient dant than it is and contributing a larger part deficiencies. to the oceanic turnover of nitrogen. Zehr’s (1995) Nitrogen fixation can occur, or has been careful exploration of these questions confirmed induced, in other non-heterocystous genera of the widespread occurrence among the Cyanobac- freshwater Cyanobacteria (Plectonema:Stewart teria of the nitrogenase-encoding DNA but that and Lex, 1970; Gloeocapsa:Rippka et al., 1971). its expression in nitrogenase activity was as The maintenance of an oxygen-free microenviron- limited as previously circumscribed. It is not ment remains a paramount precondition. One known to be expressed among the picoplanktic wayinwhich this can be achieved is through Cyanobacteria but fixers were sometimes incor- the dense adpositioning of trichomes into dense porated in the microaerophilic zones of sinking bundles or rafts (Carpenter and Price, 1976;Paerl, particulate clusters of marine snow. Expression of 1988). The effect is further enhanced by bathing nitrogenase activity among other members of the filaments in mucilage containing reducing sul- Oscillatoriales is confined to microaerophilous phydryl groups (Sirenko et al., 1968). Nitrogen conditions, which Trichodesmium is uniquely able fixation also occurs among mat-forming littoral to contrive through its own growth habit. It is species of Oscillatoria but only during darkness not relatively abundant where more nutrients when there is no photosynthetic oxygen genera- (including DIN) deny to Trichodesmium its dynamic tion (Bautista and Paerl, 1985). For many other advantage. As to why it is not more abundant in common freshwater genera (Microcystis, Woroni- thelow-DIN oceans, it was supposed, for a time, chinia, Gomphosphaeria), no such facility has been that micronutrient deficiencies (in particular, of demonstrated. iron and molybdenum) so interfere with nitro- In the marine phytoplankton, nitrogen fix- gen fixation that the otherwise obvious potential ers are represented by the non-heterocystous advantage that nitrogen fixation might confer is marine species of oscillatorialean genus of Tri- suppressed. In fact, as is now well known, rel- chodesmium. Each of the three recognised species atively high-nitrogen, low-chlorophyll regions of has adopted the life habit of forming large macro- thegreat oceans augur that the biomass capacity scopic rafts, or flakes, of uniseriate filaments. is constrained by micronutrient availability per These bundles were sufficiently prominent in the se (see Section 4.5), which access to alternative very clear tropical and subtropical seas where exploitable sources of nitrogen fails to alleviate. they mainly occur for early mariners to have Noteventhe diatom Hemiaulus, with its nitrogen- named them ‘sea sawdust’ (given the reddish- fixing endosymbiont, Richiella (Heinbokel, 1986), brown accessory pigmentation of the flakes, the is able to gain much advantage over other species name is apposite, elegantly conveying a good of the tropical gyres. The problem is still to sat- description of their appearance). Living in envir- isfy the simultaneous requirements of nitrogen onments of the Atlantic Ocean maintaining fixation. The ability to fix nitrogen really provides very low levels of inorganic combined nitro- an advantage only in those parts of the sea where gen (often <1 µMDIN), Trichodesmium thiebau- DIN is truly limiting and where energy, phospho- tii nevertheless fixes nitrogen, aerobically and rus and adequate sources of iron, molybdenum whilst photosynthesising, sufficient to satisfy the and vanadium are simultaneously sufficient to bulk of its nitrogen requirements (Carpenter and support it. McCarthy, 1975). This metabolism is energetically expensive and relatively slow but is adequate to support Trichodesmium dominance over 4.5 The role of micronutrients almost all other, nitrogen-starved phytoplankters (Carpenter and Romans, 1991;Zehr,1995). After the six elements that each contribute ≥1% This being so, it has long been puzzling to of the ash-free dry mass of phytoplankton cells ecologists why there are not more genera of (in descending order of contribution by mass, nitrogen fixers in the nitrogen-deficient oceans C, O, H, N, P, S), all the others figure in rela- or even why Trichodesmium is not more abun- tively small fractions of the cytological structure THE ROLE OF MICRONUTRIENTS 167 or participate in its function. Some of these are zinc, copper, molybdenum and cobalt are nec- used in small quantities, despite being normally essary additions to culture media (Huntsman relatively abundant in the solute content of lake and Sunda, 1980), even if the information about and sea water, where they are constitute some of their deployment and effects is difficult to inter- the major ions (Na, K, Ca, Mg, Cl). Most of the pret. For instance, the cellular content of man- remainder used by plankton cells in small quan- ganese (Mn) ranks next to that of iron. The finite tities also generally occur naturally at low con- requirement for its central role in re-reducing + centrations. These used to be known as the ‘trace P680 in photosynthesis (see Section 3.2.1)isusu- elements’ but are now more commonly referred ally fulfilled by the amounts present in lakes, to as micronutrients. which may be sufficiently abundant to bring Much of the early knowledge of the impor- about external deposition on the cell walls. In tant part played by micronutrients in the growth (unspecified) excesses of manganese ions are sup- and physiological well-being of phytoplankton posed to inhibit algal growth. Although there came not from analysisoflakeorseawater are occasional references to growth being stim- but from the attempts to grow algae in pre- ulated by the addition of manganese (Goldman, pared artificial media. The use of carefully formu- 1964), there is little evidence to suggest that the lated solutions, contrived and refined through metal is ever a significant growth-regulating fac- the experimental pragmatism of such pioneers as tor. Similar conclusions apply to zinc, copper and Chu (e.g. 1942, 1943), Pringsheim (1946), Gerloff cobalt, insofar as each participates vitally in one and co-workers (1952), Provasoli (see especially or more enzymic or cytochrome reactions. In Provasoli et al., 1957)andGorham et al. (1964; solution at concentrations >10 nmol L−1 each is see also Stein, 1973)progressively identified the seriously toxic to a majority of algae. Copper sul- additional ‘ingredients’ necessary to keep labora- phate is still widely used as an algicide (although, tory clones in a healthy, active, vegetative state. in many countries, its use in waters eventually More recently, of course, chromatographic appli- supplied for drinking is banned) and is effec- −1 cations, atomic-absorption spectroscopy and X- tive at concentrations of 0.3–1.0 mg CuSO4 L ray microanalysis have helped to confirm and (2–6 µmol CuL−1). Toxicity varies interspecifically greatly amplify the elemental composition of among algae and in relation to the organic con- planktic cells, in field samples as well as in lab- tent of the water (Huntsman and Sunda, 1980). oratory cultures, even to the specific intracellu- Possible toxic effects of redox-sensitive metal lar locations (Booth et al., 1987;Krivtsov et al., species may be magnified in relevant habitats, 1999). Yet more recently, a method for measur- including lakes subject to seasonal deep-water ing the chemiluminescence emitted in reactions anoxia, where bioavailable species may be recy- between metals and luminol appear to be both cled (Achterberg et al., 1997). precise and sensitive at very low sample concen- Clear incidences of regulation (or ‘limitation’) trations (Bowie et al., 2002). of algal activity through deficiency of these elements are scarce. In contrast, both molybdenum 4.5.1 The toxic metals and (especially) iron are known to fulfil, on occa- The known micronutrients, as they are now sions, this key limiting role in pelagic systems. understood, include several metals whose avail- The case for molybdenum has been made on a ability in natural waters may vary between defi- number of occasions (Goldman, 1960; Dumont, ciency and toxic concentrations. Some (barium, 1972). In the best-known case, additions of a vanadium) are required in such trivial amounts fewmicrograms of molybdenum per litre to that their specific inclusion in artificial culture water fromCastle Lake (in an arid part of Cal- media is considered unnecessary; their presence ifornia) were sufficient to promote, quite strik- as impurities in other laboratory-grade chemi- ingly, the growth and the attainment of a higher cals or among the solutes that leach from the standing biomass of phytoplankton, where pre- containing glassware suffices for most practical viously, despite the presence of adequate lev- purposes. On the other hand, iron, manganese, els of bioavailable P and DIN, activities had 168 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

been severely constrained (Goldman, 1960). In a than is needed by cells supplied with assimilable later investigation of the same lake, molybde- DIN to sustain the equivalent yield of cell carbon num addition was shown to stimulate carbon (Rueter and Peterson, 1987). fixation and nitrogen uptake rates, especially The iron content of phytoplankton cells is when nitrate dominated the nitrogen sources reckoned to be between 0.03% and 0.1% of ash- (Axler et al., 1980). Molybdenum is specifically free dry mass, or about 0.1–0.4 mmol Fe : mol C. involved in the nitrogen metabolism of the cell, The problem that cells have in meeting even this participating as a co-factor in the action of nitrate modest requirement lies principally in the low reductase and (in Cyanobacteria) nitrogenase, solubility of the hydrous ferric oxides that pre- and in the intracellular transport of nitrogen cipitate in aerated, neutral waters. Thus, despite (Rueter and Peterson, 1987). The cell requirement arelative abundance of total iron in fresh waters is estimated to be about 1/50 000 of that for P generally (10−7–10−5 MFe),mostofitispresentin (∼0.2 µmol Mo (molcellC)−1), which can be flocs and particulates, extremely little (≤10−15 M) accumulated from external concentrations of the being in true solution (other than at very low order of 10−11 M. According to Steeg et al. (1986), pH: Sigg and Xue, 1994). In the open oceans, the Mo deficiency nevertheless results in symptoms concentration of total iron is generally weaker of nitrogen limitation, including heterocyst for- (10−8–10−7 MFe).Particular interest has been mation among members of the Nostocales, even directed towards the eastern equatorial Pacific, though rates of nitrogen fixation are themselves thesub-Arctic Pacific and the Southern Ocean seriously impaired. (north of the Antarctic front) where concentrations are considerably lower still (perhaps 4.5.2 Iron <10−11 M) and where iron limitation of photosyn- Iron, being, by weight, the most important of thesis and growth is demonstrable (Martin, 1992; the trace components in algal cells, has long Martin et al., 1994;andseebelow). been implicated in the ecology of phytoplank- It has not always been clear just how phy- ton. The two most energy-demanding processes toplankton cells satisfy their iron needs and at in the cell – photosynthetic carbon reduction and what point these become compromised by an nitrogen reduction – involve the participation inadequacy of availability. Supplying inorganic of iron-containing compounds deployed in elec- iron to cultures and maintaining it in solution tron transport (such as ferredoxin, nitrogenase) requires the inclusion of chelating ligands, such and pigment biosynthesis. Among the recognised as citrate (Gerloff et al., 1952). It was supposed direct symptoms of iron deficiency are reduced that this role was fulfilled naturally by the humic levels of cytochrome f (Glover, 1977)andthe or fulvic acids, and that it was suitably imi- blockage of chlorophyll synthesis (and, where rel- tated by including in media formulations aque- evant, phycobilins: Spiller et al., 1982). Shortage ous extracts of soil or by substitution of repro- of iron also impairs the structural assembly of ducible solutions of nitrilotriacetic acid (NTA) thylakoid membranes (Guikema and Sherman, or trishydroxymethyl-aminomethane (tris). Proce- 1984). Thus, iron-deficient cells are able to har- dures soon standardised on the use of ethylene vest relatively fewer photons than iron-replete diamine tetra-acetic acid (EDTA, usually as its ones and photon energy is utilised less efficiently. sodium salt) in media in which cultures could Iron limitation results in poor photosynthetic be maintained over many generations. EDTA has yields of fixed carbon, lower reductive power and, proved very successful in this context. hence, an impaired growth potential. Iron defi- It seems that the large molecules of EDTA are ciencies also restrict directly the synthesis of toolarge to be absorbed directly by algae. The nitrite reductase. For active dinitrogen fixers, the role of the chelate is to maintain the source of requirement for iron is relatively greater. The iron in the medium, stably and accessibly, and synthesis of nitrogenase and the electron power which algae are then able to exploit directly, demand for the reduction of nitrogen draws through a process of ligand exchange. The upon the availability ofupto10timesmoreiron importance of providing an iron source was an THE ROLE OF MICRONUTRIENTS 169 incidental confirmation of the procedures for the dilute to support any growth of similarly-starved bioassaying of natural-water samples that became algae. Within this three-order span, results were popular in the 1960s and 1970s. The essence of erratic, either showing some or no growth but the technique is to grow a test alga, under as which could be stimulated by the addition of near-reproducible laboratory conditions as possi- Fe-EDTA or, on occasions, by EDTA alone. These ble, in water sampled from a given lake or sea performances could not be explained satisfacto- under investigation, and in samples of the same rily. Some of the variability is attributable to the water selectively enriched (‘spiked’) with the sus- difficulties of manipulating such low concentra- pected regulatory nutrients, separately and in tions, when even the impurities present interfere various combinations. Thus, the chemical compo- with the nominal interpretation. It would appear, nent that most enhanced the yield of test organ- however, that concentrations of residual TFe in ism relative to that in the unspiked water was the range 10−11 –10−10 Mmaywellbe exploitable deemed to be the capacity-regulating (‘limiting’) by some algae, provided chelators continue to factor in the original sample (Skulberg, 1964; mediate their availability. Maloney et al., 1973). The method would readily In all these cases, the maintenance of iron in confirm previous suspicions about P or N defi- solution by organic chelates is properly empha- ciencies but frequently, the tests would point sised. However, equal emphasis is due to the exis- to a direct and previously unsuspected limita- tence of a mechanism for transferring chelated tion by iron. Alternatively, the effects of N or iron in the medium into the cell. It seems most Pspikesweresubstantially enhanced when iron- likely that the uptake and assimilation of iron EDTA and therelevant spike were added to the in the cell relies on reduction of the Fe-chelate medium (Lund et al., 1975). This was true even for at or near the cell surface. In turn, this presup- water samples from particular lakes previously poses that a redox enzyme is produced close to and deliberately enriched with iron (Reynolds thecell membrane and whose action is to cleave and Butterwick, 1979). The explanation for this iron from the organic chelates adjacent to the behaviour lay almost wholly in the method and cell surface. its requirement that lake water submitted to The minimum iron requirements of active bioassay be first fine-filtered of all algal inocula nitrogen fixers must, fairly obviously, be rela- and as many bacteria as possible, prior to the tively higher than those of facultative or obli- introduction of the test organism. Reynolds et gate users of DIN. It has been suggested that al. (1981)usedserial filtrations and intermedi- dinitrogen-fixing Cyanobacteria need up to 10 ate analyses of total iron (TFe) to identify where times more iron than algae of the same species theloss of iron fertility occurred. Even coarse growing on DIN at the same rate (Rueter and filtration (50 µm) removed up to one-third of Peterson, 1987). However, Kustka et al. (2003)have the TFe (as floccular material or finer precipi- explored the complexities of iron-use efficiency tates on the algae) and glass-filter filtration (pore in the diazotrophic Trichodesmium species and cal- size 0.45 µm) removed over half of the remain- culated the fixed-carbon and fixed-nitrogen quo- der. From initial TFe concentrations close to 10−5 tas required to sustain daily growth rates of M (560 µgFeL−1), the passage of ∼10−6 M TFe 0.1 d−1. The iron use efficiency was such that iron in fine, near-colloidal suspension would nev- 1mol Fe sustained the elaboration of between ertheless sustain the subsequent growth of test 2900 and 7700 mol C d−1 (0.13–0.34 mmol algae, at least to the point of exhaustion of the Fe :mol C incorporated), thus requiring the sup- conventional N or P additions, without any fur- ply of 27–48 µmol Fe (molcellC)d−1.Tosup- ther enhancement of the iron or the EDTA. On ply the iron demand of a population equivalent the basis of further experiments, reviewed in to 0.4–4 × 10−6 molCL−1 (∼0.1–1 µgchla L−1) Reynolds (1997a), similar results were obtained requires an iron source of 1–2 ×10−10 M TFe. with iron-starved algae reintroduced into arti- It is relevant to point out that many Cyanobac- ficial media containing ≥10−8 M TFe, whereas teria (though not just the dinitrogen fixers) are media containing <10−11 Mwereconsistently too able to acquire and transport iron through the 170 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

production of extracellular iron-binding com- to iron deficiency. A part of the enhanced pounds (called siderophores) that comprise part iron pool (15–40%) supported the production of of their own high-affinity iron-transport sys- autotrophic diatoms and flagellates while the bal- tems (Simpson and Neilands, 1976). Production ance persisted (for over 40 days after fertilisation) is induced under iron stress and repressed by within the tight cyclic linkages involving pelagic its relative availability. This ability is said to con- bacteria and microzooplanktic grazers. fersome competitive advantage to Cyanobacteria We may deduce that, at least for these oceanic over other algae (Murphy et al., 1976), though this locations, the natural iron levels are simply too would seem to apply only to nitrogen fixers under low (∼10−10 M) to support any more autotrophic conditions of simultaneous nitrogen stress. biomass than they do (i.e. iron availability is abso- Piecing together the (mainly circumstantial) lutely yield limiting and it is not just nitrogen evidence, itseems scarcely likely that iron exerts fixation that is constrained). Moreover, the struc- any serious regulation on the activities of fresh- ture of typical iron-limited communities ensures water phytoplankton. Algae are exposed to rel- that bioavailable iron is retained, as far as possi- atively high concentrations of TFe supplied by ble, in surface waters. terrestrial soils and that sufficient of the iron is normally maintained in dissolved or colloidal 4.5.3 Organic micronutrients and vitamins complexes with organic carbon (DOFe) for the Besides the provision of a full spectrum of inor- carrying capacities of the nitrogen, phosphorus ganic nutrients, successive generations of sub- and light to be simultaneously iron-replete. In cultured axenic (bacteria-free) clones of many the sea, however, iron is much more dilute. species of microalgae are known to benefit Apart from fluvial inputs, concentrations are, from organic supplements at low concentrations. in part, augmented directly by wet deposition In particular, thiamine, biotin and cyanocobal- of dust, derived from arid terrestrial (aeolian) amine (vitamin B12)havebeen shown to be essen- sources (Karl, 2002), as well as from deep ocean tial nutrients to some species of algae at least. vents. In much of the sea, organic ligands prob- The reviews of Provasoli and Carlucci (1974)and ably complex sufficient of this iron to ensure its Swift (1980)highlight the widespread depen- availability to phytoplankton (again, as DOFe) but dence upon organic micronutrients among algae there remainareasof the ocean where there is of the ‘red’ evolutionary line. The centric diatoms just too little iron to avoid a deficiency of sup- and several pennate species have been shown to ply to autotrophs. It had been suggested that pro- require a supply of vitamin B12. Most dinoflag- duction in the oligotrophic ocean, long supposed ellates studied also require vitamin B12,either to be regulated by nitrogen, would be stimu- alone or in combination with thiamine or biotin lated by iron additions permitting more nitrogen or both. Among the Haptophyceae, a majority of (and thus carbon) to be fixed (Falkowski, 1997). species tested have a requirement for thiamine, In the relatively high-nutrient but iron-deficient sometimes with B12 as well. Among the Chryso- low-chlorophyll areas of the southern Pacific and phyceae, most species require the supply of two thecircumpolar Southern Ocean, subject to the or three vitamins. IRONEX fertilisation (Martin et al., 1994), it was The biochemical requirement for these sub- photosynthesis that was first stimulated by iron stances is general: thiamine is a co-factor in addition (Kolber et al., 1994). In a later fertilisa- thedecarboxylation of pyruvic acid; biotin is tion experiment in the Southern Ocean (SOIREE; a co-factor in the carboxylation and transcarb- see Bowie et al., 2001), a pre-infusion concentra- oxylation reactions of photosynthesis. Vitamin tion of 0.4 nM was raised to give a dissolved iron B12 mediates reactions involving intramolecu- concentration of 2.7 nM. This was very rapidly lar recombinations involving C---C bond cleav- depleted within the fertilised patch, to under 0.3 ages (Swift, 1980). The point is that many nM. Part of this was due to patch dilution but bacteria (including the Cyanobacteria), most adistinct biological response confirmed that the green algae and higher plants are capable of biomass limitation was exclusively attributable synthesising these products themselves and are MAJOR IONS 171 independent of an external supply. As a consequence of their metabolism, however, thiamine, biotin and cyanocobalamine are generally measurable components of the labile DOC fraction in the sea. Moreover, each is present in concentrations (equivalent to 0.5 to 5 ng C L−1:Williams, 1975)sufficient to saturate the demands of individual plankters (said to be in the order 10−12–10−10 mol L−1: Swift, 1980). The demand and supply of organic trace substances seem not to exert any strong ecological outcome on the competitive potential of plankters in the wild.

4.6 Major ions Figure 4.7 The major ionic constituents dissolved in sea water. Redrawn with permission from Harvey (1976). Although the major ions in lake and sea water (including Ca, Mg, Na, K, Cl) are no less important to planktic cells than are P, N or the micronutri- aweakacid, they allow the strongly alkaline ents, they are treated in less detail here because ions to press pH above neutrality, although this their ecological role in regulating species compo- is resisted by the presence of free carbon diox- sition and abundance is either trivial or unclear. ide in solution. Dissociation of the bicarbonate to release free CO2 serves to buffer the water 4.6.1 Cations at a mildly alkaline level, as well providing an Calcium belongs in the second of these cate- additional resource of photosynthetic DIC (Sec- gories. It doeshaveanimmediateanddirectrel- tion 3.4.1;seeFig.3.17). This crucial participation evance to the species that deploy calcium salts in the carbon-dioxide–bicarbonate system means (usually carbonate in the form of calcite) in that calcium can have a strong selective influence skeletal structures. Among the most notable of among phytoplankton that are variously sensi- these are the marine coccolith-producing hap- tive to pH and carbon sources and, ultimately, tophytes. For such organisms, there is a spe- those with an acknowledged capacity for car- cific and finite requirement for calcium but the bon concentration (CCM; see Section 3.4.2). In amounts dissolved in sea water are, globally, gen- this way, many chrysophyte species seem to be erally uniform. Of the mean solute content (35 ± confined to soft-water (low-Ca) systems (unless −1 3gkg :Section 2.2.1), calcium accounts for there are local sources of CO2 from organic fer- just over 1% by mass (typical calcium content, mentation), while many Cyanobacteria are sup- ∼0.4gL−1,i.e.∼10−2 M, or 20 meq L−1)(see posed to have an affinity for calcareous waters. Fig. 4.7). Any preference of particular species for Indeed, a large number of cyanobacterial gen- particular water massesisunlikelytobegov- era is reputed to be relatively intolerant of acid erned by differences in ambient calcium concen- conditions (pH <6.0; Paerl, 1988; Shapiro, 1990). trations. Among fresh waters, however, calcium The mechanism underpinning the observation is frequently the dominant cation (≤120 mgL−1, has not been satisfactorily explained. The gen- ≤6meqL−1), although concentrations (and spe- erality about pH sensitivity in these organisms cific ‘hardnesses’) in individual water bodies vary is doubtless confounded by the extreme toler- throughout the available range. The importance ance of high pH by many planktic Cyanobacteria, of calcium hardness resides in its relation to the yetsome species (e.g. of Merismopedia, Chroo- anions; electrochemical balance in fresh waters coccus)are plainly able to function adequately in is often contributed, substantially or in part, by notably acidic waters (pH ≥5.5; author’s observa- bicarbonate ions. Being derived from the salt of tions). The green volvocalean alga Phacotus, whose 172 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

single cells are enclosed in a calcified envelope, is dant of the four in cytoplasm. A recently pub- atruecalcicol and its presence in sediment cores lished experimental study (Jaworski et al., 2003) is taken to indicate highly calcareous phases in has reappriased the situation. The authors were the development of the lake whence the cores unable to show any dependence of the growth were extracted (Lund, 1965). rate of the freshwater diatom Asterionella on Magnesium is the second most abundant (to potassium concentrations above 0.7 µM (27.5 µg sodium) cation in sea water (Fig. 4.7)andis the KL−1), while yields were only diminished in other common divalent cation (with calcium) in cultures in which the initial concentration was freshwater. Although an essential component of below this level. Another diatom (Diatoma elonga- the chlorophylls, magnesium – a single atom is tum)andacryptomonad (Plagioselmis nannoplank- chelated at the centre ofatetrapyrolering–is tica)alsoshowednodependence on potassium not known to limit phytoplankton production in initially supplied at >0.8 µM(31µgKL−1). We nature. Supposing Mg to be under 3% of the mass may conclude that the regulation of phytoplank- of a chlorophyll molecule of 894 da, then even tongrowth by potassium or sodium is unlikely averylargephytoplankton population (1000 mg to occur naturally. chla m−3 is sustainedby30mgMgm−3,or∼1.25 It is relevant to remark briefly on another sug- µM Mg) is unlikely to challenge the availability in gestion in the early ecological literature (Pearsall, themajority of natural waters. 1922)that the species composition of the fresh- Similarly, sodium and potassium are rarely waterphytoplankton might be sensitive to the considered to have much influence on algal com- variable ratio of monovalent to divalent cations position, save through their impact on ionic (M : D). Pearsall (1922)deduced that diatoms are strength and on the effects of ionic osmosis more abundant in relatively calcareous waters across the cell membrane. Marine algae equipped (M:D< 1.5) whereas many desmids and some to deal with a medium containing some 10.7 g chrysophyceans occur in softer water. Talling and Na L−1 (i.e. ∼0.47 M, or 470 meq L−1)wouldsim- Talling (1965) showed desmids increased in major ply burst if immersed in a soft, oligotrophic lake African lakes of high alkalinity (>2.5 meq L−1) water containing between (say) 0.1 and 0.5 meq but where sodium rather than calcium is the (or 2–10 mg Na) L−1.Conversely, phytoplankters dominant cation. The observations are, broadly, from dilute fresh waters shrivel and lyse in sea upheld by later work but the underpinning mech- water. Neither would tolerate the extreme salin- anisms can be explained by sensitivity to the car- ities of certain endorheic inland waters; the dis- bon sources in the media concerned. solved sodium content of the Dead Sea is ∼1090 meq (25 g, or 1.1 mol) L−1. The cationic strength is 4.6.2 Anions compounded by some 140 meq (5.5 g) L−1 potas- Apart from the crucial behaviour of bicarbon- sium and 2540 meq (58 g) L−1 calcium. At the ate, the major anions (chloride, sulphate) do not other extreme, minimum sodium concentrations appear to limit algal production. Chloride is, by required by algae and Cyanobacteria are to be mass, the most abundant of the dissolved ions found in the literature, the highest of these being in sea water (∼19.3gL−1,i.e. ∼0.54 M, or 540 4–5 mg Na L−1 (say 0.2 meq L−1)foracultivated meq L−1)(Fig.4.7)andtheprincipal agent in its Anabaena (Kratz and Myers, 1955). However, many salinity and halinity. Among softer fresh waters, studies on other algae and Cyanobacteria report it is generally the dominant anion (0.1–1 meq much lower thresholds than this (Reynolds and L−1, 4–40 mg Cl L−1)but, elsewhere, it may be less Walsby, 1975). abundant than either bicarbonate or sulphate The requirements of phytoplankton for potas- or both. The anions influence the medium and, sium are probably similarly non-controversial. in extreme, distinguish the properties of high- This is despite its well-known importance as a chloride, high-sulphate and carbonate-hydroxyl constituent of agricultural fertilisers (acknowl- (soda) lakes. Sulphate also normally saturates the edging soil deficiencies) and, in both the sea and sulphur uptake requirements of algae down to −1 2− in many fresh waters, it being the least abundant concentrations of 0.1 meq L (4.8 mg SO4 , of the four major cations, yet the most abun- 0.05 mM). SILICON 173

In the context of sulphur biogeochemistry, In the context of the present chapter, however, this is an appropriate point to mention the bio- thefocus of interest is the extensive deploy- logical production of dimethyl sulphide (DMS). ment of silicon polymers in the scales of the This volatile compound evaporates from the sea Synurophyceae and, especially, in the skeletal to theair, where it constitutes the main natural, reinforcement of the pectinaceous cell walls of biogenic source of atmospheric sulphur. As the theBacillariophyceae (diatoms). As the diatoms molecules in the air act as condensation nuclei, are among the most conspicuous and abundant DMS production has consequences on the radia- groups represented in the phytoplankton of the tive flux to the ocean surface. In the 1980s, when sea and of fresh waters, the biological interven- the DMS fluxes were first recognised, excitement tion in the movements of silicon are of profound was engendered by the idea that the release by ecological and biogeochemical significance. Sev- marine microalgae of such a substance might eral useful reviews of this topic (e.g. Werner, contribute to the regulation of global climate. It 1977;Paasche, 1980; Sullivan and Volcani, 1981; wascited as a practical demonstration of Love- Reynolds, 1986a)appeared20to30yearsago but lock’s (1979) Gaia principle,withlivingsystems cre- more modern treatments are scarce. However, ating and regulating the planetary conditions for many aspects of the pelagic availability, uptake, their own survival. Since then, it has been recog- deployment and dynamics of silicon have been nised that the source of the DMS is a precursor well established for some time. In lots of ways, it osmolyte, dimethyl-sulphonioproponiate (DMSP), is an ideal nutrient to study. Later work has con- which is synthesised by marine microalgae and siderably amplified, rather than revolutionised, bacteria as a counter to excessive water loss. Mea- the earlier findings. surements noted by Malin et al. (1993)showedcor- Despite its chemical similarities to carbon, relations between DMS concentrations ranging the second most common element in the Earth’s between 1 and 94 nmol L−1 (mean 12) and those crust is somewhat less reactive. It occurs almost of the DMSP precursor and between the concen- invariably in combination with oxygen (as in the trations of DMSP and chlorophyll a during a sum- minerals quartz and cristobalite) and often also mer bloom of coccolithophorids in the north- with aluminium, potassium or hydrogen (kaolin- east Atlantic Ocean. The volatile DMS metabo- ite, feldspars and micas – the so-called clay miner- lite is released mainly as a consequence of the als). These are only sparingly soluble, but hydrol- operation of the marine food web (Simo, 2001). ysis of aluminium silicates, aided by mechani- Using 35S-labelled DMSP, Kiene et al. (2000)have cal weathering, allows silicon into aqueous solu- shown that DMSP supports a significant part of tion. Below pH ∼9, the dissolved reactive sili- the carbon metabolism of the marine bacterio- con available that is exploitable by diatoms and plankton and that it impinges upon the availabil- other algae is the weak monosilicic acid (H4SiO4). ity of chelated metals (see Section 4.5.2). The argu- Its upper concentration (at neutrality and 20 ◦C: ments for and against the tenancy of the Gaian ∼10−2.7 M, or ∼56 mg Si L−1)isregulated by the hypothesis of supra-organismic regulation of the precipitation of amorphous silica (Siever, 1962; planetary biogeochemistry notwithstanding, it is Stumm and Morgan, 1996). The concentrations of plain that the DMSP–DMS metabolism plays a sig- soluble reactive silicon (SRSi) that can be encoun- nificant role in the ecological structuring of the tered inmostopenfreshwaters are 1 or 2 orders oceans. lower (0.7–7 mg Si L−1, 25–250 µM); the maximal levels found in oceanic upwellings (∼3mg Si L−1)also fall within this range. In both habi- 4.7 Silicon: requirements, uptake, tats, the concentration may be drawn down substantially, as a consequence of uptake and growth deployment in phytoplankton by diatoms, by other algae, by radiolarian rhizopods and sponges. All phytoplankton have a requirement for the Uptake and intracellular transport of H4SiO4 small amounts of silicon involved in protein syn- proceed by way of a membrane-bound carrier thesis (<0.1% of dry mass; see Section 1.5.2). system that conforms to Michaelis–Menten 174 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

kinetics (Azam and Chisholm, 1976;Paasche, rect measure of the rate of recruitment of new 1980 Raven, 1983). Reported species-specific half- cells. saturation constants (KU)fortheuptake of Nevertheless, interspecific differences in size, monosilicic acid by marine planktic diatoms are shape and vacuole size determine that the generally within the range 0.3–5 µmol L−1, while amount of silicon needed to complete the new those for freshwater species are slightly higher cell varies in relation to the mass of cytoplasm (Paasche, 1980). The next steps, leading to the (and, hence, its content of C, P and N). Among precipitation of the opal-like cryptocrystalline sil- theselection of diatoms included in Tables 1.4 ica polymer used in the skeletal elements and and 1.5,Si:Cvariesbetween 0.76 and 1.42 by the species-specific morphogenesis and organi- mass (supposing the non-silica dry mass to equal sation into the punctuate plates, ribs, bracing ash-free dry mass and 50% of this to be carbon.). spars, spines and other diagnostic features that This fact is not to be confused with the differing both characterise the group and facilitate their concentrations at which various diatoms experi- identification, are closely regulated and coordi- ence growth-rate limitation by silicon availability nated by the genome of the living cell (Li and (see Section 5.4.4). Volcani, 1984;Crawford and Schmid, 1986). The Diatoms make a major impact upon the abi- resultant structures, that may survive long after otic geochemical silicon cycle. This is due partly death and which can be isolated and purified to theglobal abundance of diatoms but it is by chemical treatment, inspire the deep interest compounded by their behaviour and propensity of diatomists and taxonomists alike. Their forms to redissolve. Owing to the high density of opa- are celebrated in compendia of scanning elec- line silica (∼2600 kg m−3), most diatoms are sig- tromicrographs (for instance, Round et al., 1990), nificantly heavier than the water they displace published essentially as aids to diatom identifi- and, hence, they sink continuously. Populations cation, although they generally project a power- are correspondingly dependent upon turbulent ful artistic appeal too. It is worth emphasising entrainment for continued residence in surface that the active uptake of silicic acid is neces- waters and the loss rates through sinking remain sary not simply to sustain the amounts of sil- sensitive to fluctuations in mixed depth (see Sec- ica used in the skeleton but also to generate the tions 2.7.1, 6.3.2). Much of the production is even- saturated intracellular environment essential to tually destined to sediment out or to be eaten aid its deposition in the wall (Raven, 1983). The by pelagic consumers. Either way, there is a flux mechanism is known to be extremely effective: of diatomaceous silicon towards the abyss. Dur- external concentrations of SRSi can be lowered to ing its passage through the water column, sili- barely detectable levels (≤0.1 µmol L−1 in some cic acid is leached from the particulate material, instances: Hughes and Lund, 1962). at variable rates that relate to the size of parti- On the other hand, the cellular silicon cles, their degree of aggregation, pH and water requirement for a cell of a given species and size temperature, though probably not much exceed- is quite predictable (see Section 1.5.2 and Fig. 1.9). ing 0.1 × 10−9 mol m−2 s−1 (∼3pgSim−2 s−1) The skeletal structure in diatoms comprises two (Wollast, 1974;Werner,1977;Raven, 1983). Match- interlocking frustules,orvalves.Atcelldivision (see ing these to the sinking rates of dead diatoms Section 5.2.1), each of the daughter cells takes (many of which sink at <1md−1), the time away one of the separating maternal frustules taken to dissolve completely (200–800 d) will have and elaborates a new one to just fit inside it. The elapsed before they have settled through 1000 m amount of silicon taken up does not much differ (calculations of Reynolds, 1986a). Larger, faster- from the amount required to form the new frus- sinking centric diatoms may reach rather greater tules and it is absorbed at the time of demand. depths but the point is that very little silica This carries some negative implications for the reaches the deep ocean floor. Most will have been new cell (see Section 5.2.2)but, because no more returned to solution in the water above, and its silicon is withdrawn than is required, the rate of availability to future diatom growth is restored. It its removal from solution provides a useful indi- is easy to concur with Wollast’s (1974)viewthat SUMMARY 175

45% of the mass of siliceous debris in the sea tude more dilute in the medium than in the is redissolved between the surface and a depth living cell. They have to be drawn from the water of 1000 m. This uptake, incorporation, transport against very steep concentration gradients. Plank- and resolution of silicon from diatoms plainly ters have sophisticated, ligand-specific membrane shortcuts the abiotic movements of silicon; Wol- transport systems, comprising receptors and exci- last (1974)estimated the annual consumption of tation responses, for the capture and internal silicon by diatoms (∼12 Pg Si) reduced the resi- assimilation of target nutrient molecules from dence time of oceanic silicon from ∼13 000 to within the vicinity of the cell. These work like just a couple of hundred years. pumps and they consume power supplied by ATP In contrast, however, in the relatively trun- phosphorylation. However, cells are still reliant cated water columns of most lakes (between, say, on external diffusivities to renew the water in 5and 40 m in depth), a significant proportion their vicinities; quantitative expressions are avail- of the spring ‘bloom’ of settling pelagic diatoms able to demonstrate the importance of relative does reach the sediments intact (Reynolds and motion. The work of Wolf-Gladrow and Riebe- Wiseman, 1982;Reynoldset al., 1982b). This sell (1997)suggests that small cells may experi- does not prevent re-solution from continuing ence an advantage over larger cells in rarefied, but, once part of the superficial lake sediment, nutrient-poor water, as they are less reliant upon the rate ofsolution quickly becomes subject turbulent motion to replenish their immediate to regulation by the (usually high) external environments. concentration of silicic acid in the interstitial The uptake of nutrients supplied to starved water and by re-precipitation on the frustule planktic cells conforms to the well-tested mod- surfaces. Other substances, including organic els based on Michaelis–Menten enzyme kinetics. remains, may interfere (Lewin, 1962;Berner, Performances are characterised by reference to

1980). Thus, the pelagic diatoms become pre- themaximum capacity to take up nutrient (VUmax ) served in the accumulating sediment, providing and the external concentration (KU)that will asuperbrecord of unfolding sedimentary events half-saturate this maximum rate of uptake (i.e. overalongperiodoftimeand environmental that that will sustain 0.5 VUmax ). Clearly, a high change. In this instance, the limnetic silicon flux biomass-specific uptake rate and/or an ability to enters a highly retarded phase of its potential half-saturate it at low concentrations represent biogeochemical cycle. advantageous adaptations. Actual performances are conditioned by what is already in the cell and its ‘blocking’ of the assimilation pathways (according to the Droop ‘cell quota’ concept). A 4.8 Summary new expression (Eq. 4.12)isventured to show how theuptake rate is conditoned by the contempo- The chapter deals with the components required raneous quota. These formulations are used to to build algal cells and the means by which distinguish among uptake mechanisms that are they are obtained, given the background of some- variously ‘velocity adapted’, ‘storage adapted’ or times exceedingly dilute supplies. The materi- ‘affinity adapted’. The usage of the terms ‘limi- als are needed in differing quantities, some of tation’ and ‘competition’ (in the context of satis- which are in relatively plentiful supply (H, O, fying resource requirements) is also rationalised S), some are abundant in relation to relatively (see Box 4.1). modest requirements (Ca, Mg, Na, K, Cl), while Phosphorus generally accounts for 1–1.2% of some occur as traces and are used as such (Mn, theash-free dry mass of healthy, active cells, in Zn, Cu, Co, Mo, Ba, Va). Four elements for which theapproximate molecular ratio to carbon of failure ofsupplytosatiate demand has impor- 0.009. Minimum cell quota (q0)mayvaryinte- tant ecological consequences are treated in some specifically, generally to 0.2–0.4% of ash-free dry detail (P, N, Fe, Si). However, even the more abun- mass but some species may survive on as little dant of these nutrients are orders of magni- as 0.03%. Natural concentrations of bioavailable 176 NUTRIENT UPTAKE AND ASSIMILATION IN PHYTOPLANKTON

P (usually less than the total concentration in late winter (concentrations 50–70 µM). Temper- the water but often rather more than the sol- ate lakes and rivers may offer similar levels uble, molybdate-reactive fraction (MRP, or SRP), of resource but, again, anthropogenic activities are frequently around 0.2 to 0.3 µM. These (especially the agricultural application of nitroge- are variously augmented by the weathering of nous fertiliser) may augment these, up to 1 mM. phosphatic minerals, especially in desert catch- On the continental masses at lower latitudes ments. Forested catchments may restrict even and, especially, in arid regions, DIN losses from this supply but anthropogenic activities (quarry- catchment topsoils are small and subject to fur- ing, agriculture and tillage and, of course, the ther microbial denitrification, so that receiving treatment of sewage) may significantly augment waters are often DIN-deficient in consequence them. Asphosphorus is often considered to be (1–10 µM). the biomass-limiting constraint in pelagic ecosys- Nitrate is redox-sensitive. Ammonification is tems, P enrichment can provide a significant mediated by facultatively anaerobic bacteria. stimulus to the sustainable biomass of phyto- Ammonium is less volatile than elemental nitro- plankton. Many species can take up freely avail- gen, so DIN levels are not necessarily depleted as able phosphorus at very rapid rates, sufficient a consequence of anoxia. to sustain a doubling of cell mass in a matter Phytoplankton generally takes up DIN from of a few (≤7) minutes. The external concentra- external concentrations as low as 0.2–0.3 µM. tions required to saturate the rates of growth are Although nitrate is usually the most abundant generally under 0.13 µMPand the most affinity- of the DIN sources in surface waters, ammo- adapted species can function at concentrations nium is taken up preferentially while concen- of between 10−8 and 10−7 M. In the presence trations exceed 0.15–0.5 µMN.Half-saturation of MRP concentrations >0.1 µMP,phytoplank- of DIN uptake by small oceanic phytoplankters ton is scarcely ‘phosphorus limited’. The con- occurs at concentrations of 0.1–0.7 µMNwith clusion is supported by each of four quite dis- nitrate as substrate and 0.1–0.5 µMNwithammo- tinct approaches to determining whether cells nium. Nitrogen availability is unlikely to con- are experiencing P regulation. strain phytoplankton activity and growth before Persistent P deficiency can be countered in theDIN concentration in the medium falls to appropriately adapted species by the production below 7 µmolNL−1 (∼100 mgNm−3), in the case of phosphatase (which cleaves P from certain of large, low-affinity species, or below ∼0.7 µmol organic binders) or by phagotrophy (consump- NL−1,inthe case of oceanic picoplankton. tion of P-containing organic particles or bacteria). In the effective absence of DIN, phytoplank- Both rely on the sustained availability of these ton exploits the pool of dissolved organic nitro- alternative sources of P. gen, including urea. Certain groups of bacte- Nitrogen accounts for 7–8.5% of the ash-free ria, including the Cyanobacteria, are addition- dry mass of healthy, active cells, in the approxi- ally able to reduce (‘fix’) dissolved nitrogen gas. mate molecular ratio to carbon of 0.12–0.15. Min- The relevant enzymes operate only under anaer- imum cell quota (q0)maynotbelessthan 3% ash- obic conditions. In the Nostocales, usually the free dry mass of living cells. Nitrogen isrelatively most effective dinitrogen fixers in the freshwa- unreactive, organisms having to rely on sources terplankton, fixation is confined to specialised of the element in inorganic combination (nitrate, cells called heterocysts. They are produced fac- ammonium) but which are extremely soluble. ultatively under conditions of depleted DIN. Dif- Aggregate concentrations of dissolved inorganic ferentiation commences against a background of nitrogen (DIN) in the open sea are generally falling DIN, below 19–25 µM. It is likely that the in the range 20–40 µMbutare often depleted reaction actually responds to depletion of ammo- towardsthe surface. The most N-deficient waters nium nitrogen (to <0.5 µMNH4.N). Successful are those of the North Pacific, the Sargasso and fixation also depends upon threshold levels of the Indian Ocean. Shelf waters may be relatively light, phosphorus, iron and molybdenum being more replete, especially in temperate waters in satisfied. SUMMARY 177

In parts of the Atlantic and Indian Oceans means that the nitrogen fixers are not free to characterised by low DIN levels (often <1 µM exploit the situation. DIN), nitrogen is fixed by Trichodesmium spp. The Silicon plays a regulatory role in the plank- plankters succeed over non-fixers but dinitro- ton, not as a conventional nutrient but as a genfixers are not more widespread in DIN- vital skeletal requirement of diatoms. The crypto- deficient seas because the energy and micronu- crystalline, opal-like silica polymer that makes trient requirements are not simultaneouly up the structure of the diatom frustules is pre- satisfied. cipitated and organised within the cell from Iron is a micronutrient, the availability of thedissolved reactive monosilicic acid that the which is rarely problematic except in the large cells take up from solution. The transformations oceans. However, the amounts that occur in true between external solution, internal deposition solution are extremely small (∼10−15 M) and the and re-solution of the frustule after death are availability to algae depends upon its chelation regulated, in part, by the solubilities of the sili- by fine organic colloids. Some, at least, of this cic acid and of the silica polymer after death of fraction is accessible to phytoplankton. A total- the cell. iron (TFe) content of 10−8 Mseems adequate The amounts of silicon that are deposited in to support the needs of most species of phyto- cell walls vary interspecifically and, intraspecifi- plankton, in which iron constitutes some 0.03% cally, with size. Cell-specific silicon requirements and 0.1% of ash-free dry mass (about 0.1–0.4 range between 0.5% (in marine Phaeodactylum) mmol Fe : mol C). On the other hand, media and 37% of dry mass (in freshwater Aulacoseira); containing <10−11 Mare too dilute to support among well-studied diatoms, Si : C varies between sustained growth of algae. It seems most likely 0.76 and 1.42 by mass. Populations draw down the that minimal productivity of the relatively high- concentrations present in natural waters, from a nitrogen, low-chlorophyll areas of the Southern typical range, 25–250 µM, until depleted to half- Ocean are absolutely iron deficient. The mini- saturation levels (KU)ofabout 0.3–5 µM. How- mum iron requirements of active nitrogen fix- ever, uptake of Si scarcely exceeds the amounts ers are suggested to be relatively higher, at about deposited; silicon consumption provides an 1–2 × 10−10 M TFe. Lack of nitrogen may pre- accurate guide to the numbers of diatoms clude most other algae but lack of sufficient iron produced. Chapter 5

Growth and replication of phytoplankton

of intracellular processes leading to the comple- 5.1 Introduction: characterising tion of the cell cycle, net or otherwise of respi- growth ratory costs as specified. ‘Increase rate’(presented as rn)will be used in the context of the accu- Whereas the previous two chapters have been mulation of species-specific biomass, though fre- directed towards the acquisition of resources quently as detected by change in cell concentra- (reduced carbon and the raw materials of tion. The potential increase in the biomass pro- biomass), the concern of the present one is the vided by the frequency of cell division and the assembly of biomass and the dynamics of cell intermediate net growth of the cells of each generation will be referred to as the biomass-specific recruitment. Because most of the genera of phytoplankton either are unicellular or comprise rel- population replication rate,signified by r .Ineach atively few-celled coenobia, the cell cycle occu- instance, the dimensions relate the increment to pies a central position in their ecology. Division the existing mass and are thus expressible, in spe- of the cell, resulting in the replication of simi- cific growth units, using natural logarithms. In lar daughter cells, defines the generation. On the this way, the net rate of increase of an enlarging same basis, the completion of one full replica- population, N,inaunit time, t,isequivalent to: tion cycle, from the point of separation of one r t δN /δt = Nt/N0 = N0e n (5.1) daughter from its parent to the time that it too = divides into daughters, provides a fundamental where N0 is a population at t 0andNt is the time period, the generation time. population at time t; whence, the specific rate of Moreover, provided that the daughters are, increase is: ultimately, sufficiently similar to the parent, the rn = ln(Nt/N0)/t (5.2) increase in numbers is a convenient analogue of the rate of growth in biomass. The rate of Then, the replication rate is the rate of cell pro- increase that is thus observed, in the field as duction before any rate of loss of finished cells to in the laboratory, is very much the average of all mortalities (rL), so what is happening to all the cells present and r = r + r (5.3) is net of simultaneous failures and mortalities n L that may be occurring. The rate of increase in Replication rate is net of all metabolic losses, not thenatural population may well fall short of least those due to respiration rate (R). Where the what most students understand to be its growth computation of cytological anabolism (r)isbefore rate. Itis,therefore, quite common for plank- or after respiration and other metabolic losses tonbiologists to emphasise ‘true growth rates’ will be stated in the text. and ‘net growth rates’. In this work, ‘growth rate’ On the above basis (Eq. 5.2), one biomass (represented by r)willbeusedtorefertotherates doubling is expressed by the natural logarithm THE MECHANICS AND CONTROL OF GROWTH 179 of2(ln2= 0.693) and its relation to time pro- Results accumulated over a period of algal vides the rate. Growth rate may be expressed per change can be processed to determine the mean second but growth of populations is sometimes rate of population change over that period. Often more conveniently expressed in days. Thus, a dou- it is convenient to find the least-squares regres- bling per day corresponds to a cell replication sion of the individual counts for each species −1 rate of 0.693 d , which is sustained by an aver- ln(N1), ln(N2) ...ln(Ni), on the corresponding occa- age specific growth rate of not less than 8.0225 × sions (t1, t2 ...ti). The slope of ln(N)ont is, mani- −6 −1 10 s ,netofall metabolic and respirational festly, equivalent to rn. Much of the information losses. to be presented, in this and subsequent chapters, The present chapter is essentially concerned on the net rates of change in algal populations with the growth of populations of planktic algae, and the rates of growth and replication that may thegeneration times they occupy and the factors be inferred, is based on this approach. Modifi- that determine them. It establishes the fastest cations to this technique have been devised in replication rates that may be sustained under respect of colony-forming algae, such as Micro- ideal conditions and it rehearses their suscepti- cystis and Volvox (Reynolds and Jaworski, 1978; bility to alteration by external constraints in sub- Reynolds, 1983b). ideal environments. In most instances, information is based upon the observable rates of change in plankton populations husbanded in experi- 5.2 The mechanics and control mental laboratory systems, or in some sort of field enclosures or, most frequently, on natural, of growth multi-species assemblages in lakes or seas. They are expressed in the same natural logarithmic 5.2.1 The cell growth cycle units. Their derivation necessarily relies upon the The ‘cell cycle’ refers to the progression from application of rigorous, representative and (so far thenewly separated daughter to the point where as possible) non-destructive sampling techniques, it itself separates into daughters, allocating its to ensure that all errors due to selectivity or accumulated mass and structure between them. patchiness of distribution are minimised. Of course, the process depends upon the ade- Estimating the numbers or the biomass of quate functioning of the cell’s resource gathering each species in each of the samples provides a and organisation (Chapters 3 and 4) but it also further problem. To use such analogues as chloro- requires the accomplishment of several other key phyll, fluorescence, light absorption or scatter is assimilatory steps. The correct proteins and lipids convenient but each compounds the errors of must be formed; they have to be arranged in the sampling through misplaced assumptions about relevant cytological structures and, eventually, the biomass equivalence. They also lose a lot allocated between the pro-daughter cells. Mean- of species-specific information. There really is while, the entire nucleic acid complement has to no substitute for direct counting, using a good have been copied, the chromosomes segregated microscope and based on a pre-validated subsam- and (at least among eukaryotes) the nuclear sep- pling method, subject to known statistical confi- aration (karyokinesis)initiated. All these processes dence (Lund et al., 1958). However, the original take finite and significant periods of time to com- iodine-sedimentation/inverted microscope tech- plete. Throughout, their organisation and control nique (of Utermohl,¨ 1931) has largely given way to are orchestrated by the genome, including espe- theuse of flat, haemocytometer-type cells (Young- cially the RNA of the ribosomes. man, 1971). With the advent and improvement The regulation of the life-cycle events among of computer-assisted image analysis and recogni- eukaryotes is remarkably conserved, many of tion, algal counting is now much less of a chore. their features having analogues in the bacteria Properly used, the computerised aids yield results (Vaulot, 1995). This much is well known, the that can be as accurate as those of any human process of nuclear division having been described operator. by nineteenth-century microscopists studying 180 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.1 The cell cycle. The sketch shows the vegetative growth (G) of the new cell and, at maturity, the break into mitotic division (M) and separation of the daughter cells. Completion depends crucially upon (S) the replication of the DNA which occurs only after the regulatory proteins have been ‘satisﬁed’ that the cell has all the resources necessary to sustain the daughters. Sketch based on ﬁgures in Murray and Kirschner (1991) and Vaulot (1995), and redrawn with permission from Reynolds (1997a).

organisms as mutually disparate as yeasts and tal plates between the separating daughters: each frogs. As is also now well known, the primary has to produce and assemble the replacement alternation is, of course, between nuclear inter- parts (for details, see Pfiester and Anderson, phase, during which the cell increases in mass but 1987). The cytokinetic bequest of one parental thenucleus remains intact, and mitosis, during frustule requires each daughter diatom to pro- which the nucleus is replicated. Mitosis follows a duce anew the relevant complementary (inter- strict sequence of steps, starting with the break- nal) valve (see Crawford and Schmid, 1986,for down of the nuclear membrane (prophase); the more details). Similar issues of scale or coc- duplicated chromosomes first align (metaphase) colith replacement respectively confront divid- and then separate to the poles of the nuclear ing synurophyceaens (Leadbeater, 1990)and spindle (anaphase), before the propagated chromo- coccolithophorids (de Vrind-de Jong et al., somes become re-encapsulated in separate nuclei 1994). (telophase). The rest of the cell contents divide After separation, the next generation of around the two daughter nuclei, the original daughters resumes growth during the next maternal cytoplasm thus becoming divided to period of nuclear interphase. Following the dis- contribute the substance of each of the two new covery of Howard and Pelc (1951)that DNA syn- daughter cells, which are eventually excised from thesis is discontinuous and confined to a distinct each other to complete the cell division. It is not segment of the cell development, the interphase yet wholly clear how elaborate organelles (such as is also subdivided into corresponding the peri- flagella, vacuoles, eye-spots) are reallocated but ods. These are denoted by S, signifying synthesis, the daughters soon copy what they are miss- G1 for the preceding gap and G2 for the succeed- ing. Cell division in the markedly asymmetric ing gap, terminated by the inception of mitosis dinoflagellates allocates the armoured exoskele- prophase (see Fig. 5.1). THE MECHANICS AND CONTROL OF GROWTH 181

Assembling the growing cell has been analo- transport and protein-synthesis pathways (see gised to a factory production line, with a highly Sections 3.4.2, 4.2.2). Transcription of the relevant sensitive quality supervision over each process operon genes is stimulated by the group of cAMP (Reynolds, 1997a). Close coordination is required receptor proteins (or CRP) associated with the to sequence the events ofinterphase in the cor- active pathways. Thus, marked resource under- rect order, to check stocks and marshal the com- saturation or slow delivery are reflected in weak- ponents and, if something is missing, to deter- ened CRP flow and weakened operon activity. mine that production should be suspended. It is Much like the air-brakes on a train, active trans- also needed to initiate mitosis in a way that keeps port and synthesis act to suppress the cell’s pro- thesize of the daughter cells so evidently similar tective features but, as soon as normal functions to that of the parent cell prior to its own division. begin to fail, the mechanisms for closing non- The ‘supervision’ is, in fact, achieved through the essential processes and conserving cell materials activity of a series of regulatory proteins, knowl- are immediately expressed. Incipient starvation edge of which has developed relatively recently and the stalling of the relevant ribosomes lead to (Murray and Hunt, 1993; good summaries appear the activation of the inhibitory nucleotides, such in Murray and Kirschner, 1991;Vaulot, 1995). A as ppGpp (see Section 4.3.3). These do not just maturation-promoting factor (MPF) occurs at a arrest maturation but may induce the onset of a low concentration in newly separated daughter resting condition, with a substantial reduction cells but it increases steadily throughout inter- in all metabolic activities, including RNA and phase. Purification of MPF showed it to be made protein synthesis and respiration. The machin- of two kinds of protein. One of these, cyclin ery issaidtoremaininplaceforatleast200h B, is one of several cyclins produced and peri- after such shutdowns (Mann, 1995). If renewed odically destroyed through the cell cycle, each resources permit, however, renewed protein syn- being specific to a particular part of the cycle. thesis may be induced within minutes of their Cyclin B is the one that reaches its maximum availability. concentration at the start of mitosis. The second So long as the conditions remain benign, opti- part of the MPF is a kinase. It had been first mal functioning is supported and CRP generation discovered in a strain of mutant yeast, codified is upheld. The cell recognises that it has suffi- cdc. The mutation concerned the presence of a cient in reserve to be able to fulfil the mitosis and kinase-encoding gene, called cdc2, and the 34- so allow the DNA replication to proceed. Then, kDa kinase protein was referred to as p34cdc2. there really is no escape from the commitment. Like all kinases, it is active only when phospho- A further group of substances, called licensing rylated (cf. Section 4.2.2). In this state, it triggers factors, are bound to the chromosomes but are prophase spindle formation. After completion of destroyed during DNA replication. Licensing fac- the mitosis,thekinase is dephosphorylated and tors cannot be re-formed while the nuclear mem- the cyclinBisrapidlydegraded(byacyclinpro- brane is intact, so that the DNA synthesis can tease), thus leading to the destruction of MPF. occur only once per generation. In the daughter cells, cyclin B is synthesised Though they lack a membrane-bound nucleus again and MPF begins to accumulate for the next and any of the physical structure of a spindle division. upon which to sort the replicated chromosomes, The cues are critical. In this instance, it theprokaryotes have no lesser need than eukary- is clearly the instruction to phosphorylate the otes for a closely controlled, phased cell cycle. kinase that triggers the mitosis. The commit- At slow rates of growth, the DNA replication ment to nuclear division is, however, made ear- of E. coli occupies only a fraction of the gen- lier, when, following a sequence of signals pro- eration time, giving a delineation analogous to cessed through the preceding G1 period of inter- theG1–S–G2 phasing represented in Fig. 5.1.In phase, the DNA is finally replicated (the S phase the fast-growing Synechococcus,DNA replication in Fig. 5.1). Activation depends upon satisfaction may occupy relatively more of the cell genera- of resource adequacy, which is communicated tion time. Completion of the DNA duplication by the operons informed by the intracellularis the cue for chromosome separation and cell 182 GROWTH AND REPLICATION OF PHYTOPLANKTON

division (Armbrust et al., 1989). Cycle regulation transport and the intricacies of frustular mor- by analogues of MPF is probable. phogenesis in forming the two new frustules required to complete each cell division (see Sec- 5.2.2 Cell division and population growth tion 4.8), the actual construction of the new silica All the eukaryotic species of phytoplankton that structures is confined to a relatively short period. have been investigated conform to G1–S–G2 phas- The latter extends from just after nuclear divi- ing (Vaulot, 1995). Curiously, the best-studied sion to the point of eventual cell separation. Hav- freshwater species belong to the Chlorococcales ing passed G1 of interphase in its vegetative con- or to the Volvocales, which undergo a relatively dition, the cell commences to form the new valve prolonged growth period that is followed by a in a silica-deposition vesicle just beneath the fairly rapid series of cell divisions, resulting in plasmalemma (Drum and Pankratz, 1964). The the formation of between four (as in genera of origins of the silicon deposition vesicle and of Chlorococcales such as Chlorella and Scenedesmus) the control of the highly species-specific pattern- to 16 or 32 (in Eudorina)or,perhaps, as many ing of the new valves are described in detail in as 1000 (Volvox itself) daughter cells. Suppressed Pickett-Heaps et al.(1990). The trigger for the pro- though the smooth transition between genera- cess is DNA replication. Thus, no new wall forms tions may be, it is also quite evident that, over without the initiation of the nuclear division. two or three generations, the increase in specific Equally, the commitment to division is taken biomass adheres closely to a smooth exponen- before the parent cell has taken up sufficient sol- tial rate (Reynolds and Rodgers, 1983). Reynolds’ uble reactive silicon either to fulfil the skeletal (1983b)deductions on the increase in biomass of demand of the cell division, or to be able to main- afieldpopulation of Volvox aureus are also contain the necessary internal concentration (Raven, sistent with a smoothing of both cell growth 1983). This carries ecological consequences: if the and population growth with respect to the cell- requirement is pitched against low or falling division sequence. To treat the growth rate and external concentrations of monosilicic acid, it thetimes of consecutive generations (tG)inthe is possible that, in a growing population, cells same terms as simple binary fission times may begin division in a silica-replete medium but be cautiously justified. Based on Eq. (5.2), we encounter deficiency before it is completed. Many deduce: cells may fail to complete the replication and die (Moed, 1973). r = ln 2(t )−1 (5.4) G While external concentrations continue to −1 On the other hand, every confidence can be satisfy uptake requirements (KU: 0.3–5 µmol L ; accorded to deductions about the observable rate Section 4.7), the demand is assuaged and the of population growth over consecutive genera- completion of the next generation can reason- tions of diatoms. There is a manifest similarity ably be anticipated. For all phytoplankton, the of size between parent and daughter cells, owing processes of gathering of raw materials equiva- to the shared bequest of the parental frustules. lent to its current mass, of assembling them into The cellular requirements of each species are also species-specific proteins and lipids and, then, into remarkably constant, at least when cell size is the correct cytological structures and organelles, taken into account (Lund, 1965;seeTables 1.4, each occupy a finite period of time. Once accom- 1.5). Cells take up little more monosilicic acid plished, further time is required for the com- than they require to sustain the skeletal demands pletion of the S, G2 and mitosis phases, prior of the imminent division (Paasche, 1980), includ- to the occurrence of the final cytokinetic sepa- ing that needed to maintain the necessary inter- ration. As stated above, this event or, at least, nal concentration (see Section 4.7). These char- thefrequency with which it occurs, is of fun- acters lend themselves to accurate computation damental significance to the plankton ecologist. of biomass increase from the division of cells To predict, measure accurately or model the and its direct analogy to silicon uptake (Reynolds, rate of growth of cells has long been an ambi- 1986a). Despite the complicated kinetics of sil- tion of students of the phytoplankton. Most of icon uptake, the constraints on intracellular the convenient, traditional determinations of the THE DYNAMICS GROWTH AND REPLICATION 183 measured rates of change in numbers are, of be increasing rapidly and, generally, will be dou- course, surrogates ofcellgrowthandtheyare bling its mass at approximately regular intervals. always net of metabolic losses and, often, also net It is early in this exponential phase that the max- of mortalities of replicated cells. The rates of cell imal rate of replication is achieved, when r is replication are rarely predictable from separate supposed to be equal to the observed net rate determinations of the capacities deduced from of increase, rn,solvedbyEq.(5.2). Later, as the experimental measurements of photosynthetic resources in the medium become depleted or the rate or nutrient uptake rate (although these rep- density of cells in suspension begins to start self- resent upper limits). It is easy to share the frustra- shading, the rate of increase will slow down con- tions of all workers who have struggled with the siderably (eventually, the stationaryphase). Care is problem of the determination of in-situ growth taken to discount the biomass increase in this rates. phase from the computation of the exponent of the maximum specific growth rate, r . The fastest published rate of replication for 5.3 The dynamics of phytoplankton any planktic photoautroph is still that claimed growth and replication in for a species of Synechococcus (at that time named controlled conditions Anacystis nidulans)byKratz and Myers (1955). Atatemperature of 41 ◦C, the Cyanobacterium increased its mass 2896-fold in a single day, There is another way to address the potential through the equivalent of 11.5 doublings (tG = ratesofcell replication of phytoplankton and 2.09 h), and sustaining a specific rate of expo- that is through the dynamics of isolates under nential increase (r )of7.97 d−1 (or 92.3 × 10−6 and carefully controlled conditions in the labora- s−1). Numerous other algal growth rates are tory. Wemight begin by assessing how well the recorded in the literature cover wide ranges cells of a given species perform under the most of species, culture conditions and temperatures. idealised conditions it is possible to devise. Once Several notable attempts to rationalise and com- an optimum performance is established, further pile data for interspecific comparison include experiments may be devised to quantify the influ- those by Hoogenhout and Amesz (1965), Reynolds ences of each of the suspected controlling fac- (1984a, 1988a) and Padisak´ (2003). The selection of tors. Finally,thevarious impositions of sub-ideal entries inTable5.1 is hardly intended to be com- growth conditions can be evaluated. The follow- prehensive but it does refer to standardised meas- ing sections apply this approach to a selection of urements, made at or extrapolated to 20 ◦C, on a freshwater species of phytoplankton. diversity of organisms of contrasting sizes, shapes and habits. The temperature is critical only inso- 5.3.1 Maximum replication rates as a farasitisuniform and that it has been a popular function of algal morphology standard among culturists of microorganisms. It The collective experience of culturing isolates of is probably lower than that at which most indi- natural phytoplankton in the laboratory has been vidual species (though not all) achieve their best summarised by Fogg and Thake (1987). The fastest performances (see Section 5.3.2 below). rates of species-specific increase are attained in The entries in Table 5.1 show a significant prepared standard media, designed to saturate range of variation (from ∼0.2 to nearly 2.0 d−1). resource requirements, when exposed to con- There is no immediately obvious pattern to the stant, continuous light of an intensity sufficient distribution of the quantities – certainly not to saturate photosynthesis, and at a steady, opti- one pertaining to the respective phylogenetic mal temperature. Even then, maximal growth affinities of the organisms, nor to whether they rates are notestablished instantaneously. There are colonial or unicellular. The variations are is usually a significant ‘lag phase’ during which not random either, for in instances where more theinoculated cells acclimatise to the ideal world than one authority has offered growth-rate deter- into which they have been introduced. Within a minations for the same species of alga, the day or two, however, the isolated population will mutual agreements between the studies has been 184 GROWTH AND REPLICATION OF PHYTOPLANKTON

−1 Ta b l e 5.1 Maximum speciﬁc growth rates (r20 d )reported for some freshwater species of phytoplankton in laboratory cultures, under continuous energy and resource saturation at 20 ◦C

−1 Phylum Species r20 d References Cyanobacteria Synechococcus sp. 1.72a Kratz and Myers (1955) Planktothrix agardhii 0.86 Van Liere (1979) Anabaena flos-aquae 0.78 Foy et al.(1976) Aphanizomenon flos-aquae 0.98 Foy et al.(1976) Microcystis aeruginosab 1.11 Kappers (1984) Microcystis aeruginosac 0.48 Reynolds et al.(1981) Chlorophyta Chlorella strain 221 1.84 Reynolds (1990) Ankistrodesmus braunii 1.59a Hoogenhout and Amesz (1965) Eudorina unicocca 0.62 Reynolds and Rodgers (1983) Volvox aureus 0.46 Reynolds (1983b) Cryptophyta Cryptomonas ovata 0.81a Cloern (1977) Eustigmatophyta Monodus subterraneus 0.64a Hoogenhout and Amesz (1965) Chrysophyta Dinobryon divergens 1.00 Saxby (1990), Saxby-Rouen et al. (1997) Bacillariophyta Stephanodiscus hantzschii 1.18 Hoogenhout and Amesz (1965) Asterionella formosa 1.78 Lund (1949) Fragilaria crotonensis 1.37 Jaworski, in Reynolds (1983a) Tabellaria flocculosa var. asterionelloides 0.66 G. H. M. Jaworski (unpublished data) Dinophyta Ceratium hirundinella 0.21 G. H. M. Jaworski (unpublished data)

a Rate extrapolated to 20 ◦C. b Unicellular culture. c Colonial culture.

generally excellent (Reynolds, 1988a, 1997a). replication rates shown in Table 5.1 (save the Where there has been a significant departure, as entry for Dinobryon that was not available to the there is inthecaseofthe two entries for Micro- 1989 compilation) and the corresponding species- cystis,itisattributable to the difference between specific surface-to-volume ratios noted in Table working with a colonial strain and, as is com- 1.2,isreproduced in Fig. 5.2. The regression line mon among laboratory cultures, one in which fitted to points plotted in Fig. 5.2 is: the colonial habit had been lost. This turns out = . / 0.325 −1 to be an important observation, for it provides r20 1 142(s v) d (5.5) theclue to the robust pattern that accounts foralargepartof the variability in organis- where s is the approximate area of the algal sur- mic replication rate, which relates to organismic face (in µm2)andv is the corresponding vol- morphology. The apparent dependence of growth ume (in µm3). Both dimensions were estimated rate on algal size and shape, suggested by ear- from microscope measurements and the com- lier analyses (Reynolds, 1984a)wasconvincingly pounding of relevant geometric shapes (Reynolds, confirmed when the replication rates (r20)were 1984a). The coefficient of correlation is 0.72; thus, plotted against the surface-to-volume ratio (sv−1) 52% of the variability in the original dataset is ratio of the life-form,regardless of whether it was explained. aunicell,coenobium or mucilage-bound colony The outcome is instructive in several ways. (Reynolds, 1989b). The relationship, between the First, it is satisfying that surface-to-volume THE DYNAMICS GROWTH AND REPLICATION 185

volume. It was pointed out first by Lewis (1976) that the morphologies of marine phytoplankton, despite embracing a range of sizes covering 6 or 7orders of magnitude, are such that many of the larger ones are sufficiently non-spherical for the corresponding surface-to-volume values to vary only within 2. He deduced that this conservatism of (sv−1)was not incidental but a product of natural selection. When Reynolds (1984a) attempted theanalogous treatment for a selection of fresh- waterphytoplankton, nearly 3 orders of magnitude of variation in (sv−1)were found, against over 9 orders of variation in the corresponding unit volumes (see 1.7). The cytological relation- Figure 5.2 Maximum growth and replication rates of ship of cell surface to cell mass is clearly a rele- phytoplankters in continuously light- and nutrient-saturated ◦ vant factor in cell physiology. media at constant temperatures of 20 C, plotted against their The second interesting feature of Fig. 5.2 is the respective surface-to-volume ratios. The algae are: An flo, / Anabaena flos-aquae; Aphan, Aphanizomenon flos-aquae; Ast, slope of r20 on (s v): the exponent, 0.325 agrees Asterionella formosa; Cer h, Ceratium hirundinella; Chlo, Chlorella closely with Raven’s (1982)theoretical argument sp.; Cry ov, Cryptomonas ovata; Eud, Eudorina unicocca; Fra c, forgrowth conforming to a model relationship − Fragilaria crotonensis; Mic, Microcystis aeruginosa; Monod, of the type, r = a constant × (cell C content) 0.33. Monodus sp.; Monor, Monoraphidium sp.; Pla ag, Planktothrix Raven’s supposition invoked the slower increase agardhii; Ste h, Stephanodiscus hantzschii; Syn, Synechococcus sp.; of surface (as the square of the diameter) than Tfl, Tabellaria flocculosa; Volv, Volvox aureus. The fitted thevolume (as its cube) of larger-celled organ- least-squares regression is r = 1.142 (s/v) 0.325. Redrawn 20 isms. Assuming, for a moment, carbon content with permission from Reynolds (1997a). to be a direct correlative of protoplasmic volume (as is argued in Section 4.2), and the sur- should provide such a strong allometric state- face area to be a 2/3 function of increasing vol- ment about the capacity of the alga to fulfil its ume, then the arithmetic of the indices to (s/v) ultimate purpose. The empirical relation between clearly sum to 1/3. Raven’s (1982) derivation dif- these two attributes is, of course, not constant, fers from the more frequently quoted deduction even among individual spherical cells. Rather, it of Banse (1976), namely r = a constant × (cell C diminishes with increasing diameter (d), with a content)−0.25, which had been based upon marine slope of exactly 2/3. The unit in which (sv−1)is diatoms. Reynolds’ (1989b)equation (i.e. that in expressed, (µm2/µm3 =) µm−1, has the dimen- Fig. 5.2)isnot necessarily at odds with Banse’s sion of reciprocal length and conveys the idea findings, as the assumption of a constant rela- that the decline in assimilation and growth effi- tionship of C to external cell volume does not ciency might be primarily a function of the hold for the (larger) diatom cells characterised intracellular distance that metabolites must be by large internal vacuolar spaces. conducted within the cell. The implication is A further satisfaction about the relationship that small spherical cells are metabolically more comes from the fact that the scatter of points active than large ones. If there is to be an advan- shown in Fig. 5.2 becomes a cluster at the end tage in being larger, it must either be at the of the regression line fitted by Nielsen and Sand- expense of the potential for rapid growth, or Jensen (1990)tothegrowthratesofhigherplants it should invoke a simultaneous distortion in as a function of their surface-to-volume ratios. shape. As the sphere is bounded by the least pos- The slopes of the two regressions are almost iden- sible surface enclosing a given three-dimensional tical. Presumably, small size, the consequent rel- space, any distortion from the spherical form atively high surface-to-volume ratio, structural increases the surface area relative to the enclosed simplicity and the exemption from having to 186 GROWTH AND REPLICATION OF PHYTOPLANKTON

allocate resources to the production of mechan- plotting (Fig. 5.3), data were normalised by relat- ical and conducting tissues provide the main ing the logarithm of daily specific replication rate reasons for the high rates of specific biomass at the given temperature, log(rθ ), to the given increase among planktic microalgae relative to temperature (θ ◦C) rendered on an Arrhenius those of littoral bryophytes and angiosperms. scale. The latter invokes the reciprocals of abso- The ability of the plankter to exchange materials lute temperature (in kelvins). Thus, 0 ◦C (or 273 K) across and within its boundaries is a key determi- is shown as its reciprocal, 0.003663. For manipu- nant of its potential physiological performance. lative convenience, the units shown in Fig. 5.3a That ability is strongly conditioned by the ratio are calculated in terms of A = 1000 [1/(θK)]. The of its surface to its volume. thousand multiple simply brings the coefficient into the range of manageable, standard-form 5.3.2 The effect of temperature numbers. Sourcing from the various literature compi- In this format, the temperature-response plots lations mentioned in the previous section, reveal several interesting features. These include Reynolds (1984a)deduced that, with the excep- interspecific differences in the temperature of tion of acknowledged cold-water stenothermic maximum performance, ranging from appearing and thermophilic species, most laboratory strains at a littleover20◦C(alittle under 3.42 A) in Apha- of planktic algae and cyanobacteria then tested nizomenon flos-aquae and Planktothrix agardhii (orig- achieved their maximal specific rates of replica- inal data of Foy et al., 1976) but somewhere >41 ◦C tion in the temperature range 25–35 ◦C. A few (<3.19 A)intheSynechococcus of Kratz and Myers (like the Synechococcus of Kratz and Myers, 1955) (1955). The differences in the normalised parts maintain an accelerated function beyond 40 ◦C of the species-specific slopes reflect interspecfic but, exposed to their respective supra-optimal differences in sensitivity to variation in tempera- temperatures, the replication rates of most of ture. Thus, the slope fitted to the data for Synecho- the species considered here first stabilise and, coccus,for example, has the value β =−3.50 A−1. ◦ sooner or later, fall away abruptly. From 0 Cto Cast in the more traditional terms of the Q10 just below the temperature of the species-specific expression for the factor of rate acceleration over optimum, the replication rates of most plankters a10-◦Cstepincustomary temperature (usually in culture appear, as expected, to increase expo- that from 10 to 20 ◦C), the normalised response nentially as a function of temperature. However, has a Q10 of ∼2.6. In contrast, the slope for colo- −1 thedegree of temperature sensitivity of the div- nial Microcystis, β =−8.15 A (Q10 ∼ 9.6), reveals ision rate is evidently dissimilar among plank- arelatively greater temperature sensitivity. The ters. In some, growth rates vary byafactor of ∼2 slopes, of course, reflect interspecific differences for each10◦Cstepintemperature, as Lund (1965) in the sum of metabolic responses to tempera- recognised; for others, the temperature depen- ture fluctuation, some of which are themselves dence ofgrowthrateismoresensitiveandthe differentially responsive to thermal influence. slope of r on temperature is steeper. Whereas, for instance, photosynthetic electron ◦ Seeking some general expression to describe transfer has a Q10 of approximately 2 over a 30 C thesensitivity of algal replication rates to temper- Range (see Section 3.2.1) and both light-saturated ature, Reynolds (1989b)usedthesame data com- photosynthesis and dark respiration carry Q10 val- pilations to identify sources of relevant informa- ues in the range 1.8–2.25 (Section 3.3.2), protein tion on growth performances. What was needed assembly has a Q10 said to exceed 2.5 (Tamiya were the maximum rates of replication of named et al., 1953). Whereas the rates of growth of the algal species maintained in culture under con- plankters whose (relativly gentler) slopes appear stant, photosynthesis-saturating light conditions towards the top ofFig.5.3amight reflect tem- and initially growth-saturating levels of nutrients perature constraints on individual assembly pro- but at two or (ideally) more constant tempera- cesses, the (steeper) slopes towards the bottom tures. Data satisfying this criterion were found of the figure refer to larger, low (s/v)forms for 11species.Forthe purpose of comparative and coenobial Cyanobacteria whose responses THE DYNAMICS GROWTH AND REPLICATION 187

of temperature sensitivity of replication (β,from Figure 5.3 Temperature dependence of light-saturated Fig. 5.2a) against the corresponding organismic −1 growth in a selection of freshwater phytoplanktic species. (a) (sv )value. β is a significant (p < 0.05) correlative Datasets normalised against a temperature on an Arrhenius of the surface-to-volume attributes of the eleven scale (103/K); (b) the slopes of the regressions plotted algae tested. The regression, β = 3.378 − 2.505 against the surface-to-volume ratios of the algae. The algae log (sv−1), has a coefficient of correlation of 0.84 are: Ana, Anabaena flos-aquae; Ana cyl, Anabaena cylindrica; Ank, and explains 70% of the variability in the data. Ankyra judayi; Aph, Aphanizomenon; Ast, Asterionella formosa: The open circles entered in Fig 5.3aarenot part Coel, Coelastrum microporum; Cry er, Cryptomonas erosa; Cry ov, of the generative dataset but come from a previ- Cryptomonas ovata; Dict, Dictyosphaerium pulchellum; Fra c, Fragilaria crotonensis; Lim r, Limnothrix redekei; Mic, Microcystis ously untraced paper of Dauta (1982) describing aeruginosa; Monor, Monoraphidium sp.; Ped b, Pediastrum thegrowth responses of eight microalgae. They boryanum; Pla ag, Planktothrix agardhii; Sc q, Scenedesmus have been left as a verification of the predictive quadricauda; Syn, Synechococcus. The least-squares regression value of the regression. inserted in (b) is fitted only to the solid points; its equation is The hypothesis that algal morphology also −1 β = 3.378 –2.505 log (sv ). Redrawn with permission from regulates the temperature sensitivity of the Reynolds (1997a). growth rate is not disproved. For the present, β can be invoked to predict the growth rate of an are determined by the temperature sensitivity of alga of known shape and size at a give tempera- the slowest processes of intracellular assimilation ture, θ,following Eq. (5.6): and relative rates of surface exchange (Foy et al., 1976;Konopka and Brock, 1978). log(r ) = log(r ) + β[1000/(273 + 20) This pattern of behaviour is emphasised in θ 20 −1 the plot(inFig.5.2b) of the species-specific slopes − 1000/(273 + θ)]d (5.6) 188 GROWTH AND REPLICATION OF PHYTOPLANKTON

5.3.3 Resourcing maximal replication (1990) calculated a possible carbon delivery rate − − − That the slowest anabolic process should set of 35.7 × 10 6 gC(gcell C) 1 s 1. This is suffi- thefastest rate of growth leads to an impor- cient to meet the full growth requirement in 19 tant corollary of concern to the ecologist. It is 416s,orabout 5.4 h. Interestingly, it is also pos- simply that it cannot be obtained without each sible to deduce, from the number of photosyn- of its resource requirements being supplied at thetic reaction centres represented by 1 g chla demand-saturating levels. At steady state, the rate (between 2.2 and 3.4 × 1018 ) (see Section 3.2.1) ◦ of photosynthesis and the rates of uptake of each and their operational frequency at 20 C(∼250 − of its nutrients match the growth demand. More- s 1), that photosynthetic electron capture might − over, aspointed out in Chapters 3 and 4,thepho- proceed at between 0.55 and 0.85×1021 (g chla) 1 − tosynthetic and uptake systems carry such excess s 1. The potential fixation yield is thus between capacity that they can sustain higher demands 0.07 and 0.11 × 1021 atoms of carbon per second, − than those set by maximum growth rate. This or between 0.11 and 0.18 ×10 3 mols carbon per − − is not to deny that the demands of cell replica- (g chla) 1 s 1,oragain,between 4.9 and 7.6 mg C − − tion might not at times exceed the capacity of (mg chla) 1 h 1.Putting C : chla = 50, a carbon − the environment to supply them or that growth delivery rate of between 27 and 42 × 10 6 gC(g − − rate might not, indeed, fall under the control cell C) 1 s 1 may be proposed, which, again, is of (become limited by) the supply of a given well up to supplying the doubling requirement resource. Following this logic, we can nominate in something between 4.6 and 7.1 h (Reynolds, the demandforresources (D)setbythesustain- 1997a). The calculations suggest that photosyn- able growth rate and compare this with the abil- thesis can supply the fixed-carbon requirements ities of the harvesting mechanisms to perform of the dividing cell in a little over half of the gen- against diminishing supplies (S). eration time. However, they make no allowance As a case in point, the Chlorella strain used for respirational or other energetic deficits (see in the analysis of growth rate (Table 5.1 and Section 5.4.1 below). Reynolds, 1990)achieved consistently a maximal For comparison, the well-resourced Chlorella rate of biomass increase of 1.84 d−1 at 20 ◦C. cell has no problem in gathering the carbon diox- Given the size of its spherical cells (d ∼4 µm; ide to meet the photosynthetic requirement. The s ∼50 µm2; v ∼33 µm3), this is faster than is pre- diffusion rate calculated from Eq. (3.19)insec- dicted by the Eq. (5.6)oftheregression (Fig. 5.2), tion 3.4.2 indicated that delivery of the entire = . ∼ which gives r20 1 31. Staying with the real data, doubling requirement of carbon in 2300 s (i.e. one biomass doubling (taken as the equivalent just over 38 minutes). In order to maintain of an orthodox cell cycle culminating in a sin- steady internal Redfield stoichiometry, the grow- − gle division) defines the generation time; by re- ing cell must absorb 9.43 × 10 3 mol P (mol −1 / arrangement of Eq. (5.3), tG = 9.05 h. During this Cincorporated) per generation (i.e. 1 mol 106 period of time, the alga will have taken up, assim- mol C). The phosphorus requirement for the dou- − ilated anddeployed1gofnewcarbonforevery1 bling of the cell-carbon content of 0.63 × 10 12 − − gofcellcarbonexistingatthestart of the cycle. mol is 5.9 × 10 15 mol P cell 1, which, at its maxi- − It is not assumed that the increase in biomass mal rate of phosphorus uptake (13.5 × 10 18 mol − − is continuously smooth but the average exponen- Pcell 1 s 1 (Fig. 4.5), the cell could, in theory, tial specific net growth rate over the generation take up in only 0.44 × 103 s, that is, in just 7.3 time is (1.84/86 400 s =)21.3× 10−6 s−1. This, in minutes! Note, too, that an external concentra- − − turn requires the assimilation of carbon fixed in tion of 6.3 × 10 9 mol L 1 is sufficient to supply photosynthesis at an instantaneous rate of 21.3 theentire phosphorus requirement over the full × 10−6 gC(gcell C)−1 s−1.Fromthemaximum generation time of 9.05 h (see Fig. 4.6). Solving measured photosynthetic rate at ∼20 ◦C[17.15mg Eq. (4.12)forthesupplyofnitrogentothesame −1 −1 O2 (mg chla) h ]and,assuming a photosyn- cell of Chlorella,aconcentration of 7 µmol DIN −1 ∼ × −18 −1 thetic quotient of 1 mol C : 1 mol O2 (12gC:32 L should deliver 175 10 mol N s , suf- gO2)andaC:chla of 50 by weight, Reynolds ficient to fulfil the doubling requirement of REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 189

(0.151 × 0.63 × 10−12 =) 0.095 × 10−12 mol N calculations in Section 5.3.3,that growth perfor- in 540 s (9 minutes). mance is most vulnerable to interruptions to net These calculations help us to judge that, for photosynthetic output and the supply of reduced- the rateofcellgrowthtoqualify for the descrip- carbon skeletons to cell assembly. It is self-evident tion ‘limited’, whether by light or by the avail- that photoperiod truncation by phases of real or ability of carbon, phosphorus or any other ele- effective darkness must eventually detract from ment, then it has to be demonstrable that the the ability to sustain rapid growth. For small generation time between cell replications is pro- algae, even maintaining any adequate reserve of longed. Moreover, it has to be shown that the condensed photosynthate (such as starch, glyco- additional time corresponds to that taken by the gen, paramylum, etc.) soon becomes problematic cells of the present generation to acquire suffi- during extended periods of darkness, whereas all cient of the ‘rate-limiting’ resource to complete light-independent anabolism will become rapidly the G1stageandthus sustain the next division. starved ofnewlyfixed carbon. Of the responses to light/dark alternation that might be anticipated, the most plausible is 5.4 Replication rates under that the rate of cell replication becomes a direct sub-ideal conditions function of the aggregate of the light periods. If the cell required a 24-h period of continuous light exposure in which to complete one genera- The corollary of the previous section is that tion, then, other things being equal, a day/night the achievement of maximal growth rates is alternation of 12 h should determine that at least not dependent upon maximal photosynthetic two photoperiods must be passed (not less than rates and nutrient uptake rates being achieved: 36 h real time) before the cell can complete its the resource-gathering provisions have capacity replication. By extension of this logic, day/night in excess over the heaviest resource demands alternations giving 6 h of light to 18 h of dark- of growth. This luxury can be enjoyed only ness, or 3 h to 21 h will each double the real under ideal conditions of an abundant supply of time of replication. We may note that, on the resources, which scarcely obtain in the natural basis of this logic, alternations of6hlightto environments of phytoplankton: darkness alter- 6hdark(or,for that matter, 1-minute alterna- nates with periods of daylight, depth is equated tions from light to dark) should not extend the with (at best) sub-saturating light levels and a bal- generation time beyond the 12-h cycle of alter- anced, abundant supply of nutrients is extremely nations. rare. The question that arises relates to the lev- Surprisingly, there is not a lot of experimen- els at which resources start to impose restric- tal evidence to confirm or dismiss these conjec- tive ‘limitations’ on the dynamics of growth. The tures. Although there are indications that the question is not wholly academic, as it impinges logic is neither ill-founded nor especially unre- on the prevalent theories about competition for alistic, it does exclude two influential effects. light and nutrients. Some, indeed, may need revi- One is the ongoing maintenance requirement sion, while growth-simulation models founded of the cell – all those phosphorylations have upon resource harvesting are likely to be erro- to be sustained! The power demand, which per- neous, except at very low nutrient levels. sists through the hours of darkness and light, is met through the respirational reoxidation of 5.4.1 The effect of truncated photoperiod carbohydrate. Unfortunately, it is still difficult Perhaps the most obvious shortcoming that real to be certain about precisely how great that habitats experience in comparison with idealised demand might be, at least partly because of his- cultures is the alternation between light and toric difficulties in making good measurements dark: this is avoidable in nature but only at polar and, in part, because sound testable hypotheses latitudes and, even then, for just a short period about maintenance have been lacking (see Sec- of the year. It also seems likely, following the tions 3.3.1, 3.3.2 and 3.5.1). Most of the available 190 GROWTH AND REPLICATION OF PHYTOPLANKTON

information about the respiration rates of plank- excretion, or photorespiration (see Section 3.3.4), tic algae and Cyanobacteria comes from the ‘dark the carbon losses from cells must be expected controls’ to experimental measurements of pho- often to exceed basal metabolism. The experi- tosynthetic rate (of, for instance, Talling, 1957b; ments of Peterson (1978)show how easily the Steel, 1972;Jewson,1976;Robarts and Zohary, coupling between respiration and growth is bro- 1987). Rates, appropriately expressed as a propor- kenand why the fractions of photosynthetic pro- tion of chlorophyll-specific Pmax,typically range duction lost to respiration, reported in the liter- between 0.04 and 0.10, over a reasonable range ature (reviewed by Tang and Peters, 1995), are so of customary temperatures. Translating from the variable. chlorophyll base to one of cell carbon, Reynolds The second reservation about extrapolating (1990)deduced specific basal metabolic rates for growth over summated photoperiods concerns Chlorella, Asterionella and Microcystis at 20 ◦Cof thephotoadaptation of cells. Culturing cells (respectively) 1.3, 1.1 and 0.3 × 10−6 mol C (mol under ideal irradiances actually tends to lead to a cell C)−1 s−1. These fit sufficiently well to a regres- reduction in the cell-specific chlorophyll content, sion parallel to the one describing maximal repli- often to as little as 4 mg (g ash-free dry mass)−1; cation rate (Eq. 5.4,Fig.5.2), that it is possible to Reynolds, 1987a;C:Chl∼100). On the other ◦ hypothesise that basal respiration at 20 C(R20) hand, populations exposed to low light intensi- conforms to something close to: ties are able to adapt by increasing their pigment content (see Section 3.3.4). It is almost as if the R = 0.079(sv−1)0.325 (5.7) 20 cell’s photosynthetic potential varies to match In this case, R is roughly equivalent to 0.055 r . the growthrequirement, rather than the oppo- Moreover, there is no apriori reason to suppose site, as is generally presumed. Turning off the that basal respiration rate necessarily carries a light for a part of the day provokes photoadap- temperature sensitivity different from other bio- tative responses in respect of the shortened pho- chemical processes in the cell (that is, Q10 ∼ 2). It toperiod to the extent that the energy available is suggested, again provisionally, that the propor- to invest in growth, normalised per light hour, is tionality of Eq. (5.6) holds at other temperatures, compensated, as shown by the data of Foy et al. i.e. Rθ ∼ 0.055rθ . (1976)(seeFig. 3.16). In the context of growth, however, the value There are limits to this argument, of course. is academic rather than deterministic, for it is On the other hand, the abilities of certain by no means proven that the basal respiration diatoms (Talling, 1957b;Reynolds, 1984a) and, applies equally in the light and in the dark. The especially, of some of the filamentous Cyanobac- implication of photosynthetic quotients (PQ)of teria, such as Planktothrix (formerly Oscillatoria) 1.1–1.15 (Section 3.3.2)isthat 10–15% more oxy- agardhii (Jones, 1978;FoyandGibson, 1982;Post gen isgenerated in photosynthetic carbon fixa- et al., 1985)tofunction on very low light doses tion than is predicted by the stoichiometric fixed- has been well authenticated. The curves plotted carbon yield and that the ‘missing’ balance repre- in Fig. 5.4 represent a selection of experimen- sents respirational losses in the light. Ganf (1980) tally derived fits of specific growth rates of named observed that when Microcystis colonies were phytoplankters at 20 ◦Cincultures fully acclima- transferred from zero to saturating-light inten- tised to the daily photon fluxes noted. Far from sities, their respiration rate accelerated rapidly, being a linear function of light dose, except at −1 −1 from ∼25 to ∼50 µmol O2 (mg chla) h ,and very low average photon fluxes, the more adapt- did not fall back until after the colonies had able species are able to increase biomass-specific been transferred back to the darkness. The time photosynthetic efficiency so that the growth taken to return to base rate was proportional demand can continue to be saturated at signif- to thetime spent at light saturation. Insofar icantly lowered light intensities. as the same inability to store excess photosyn- How far the photosynthetic apparatus can thate requires some homeostatic defence reac- be pushed to turn photons into new biomass tion, such as accelerated respiration, glycolate is ultimately dependent upon the integrated REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 191

Figure 5.5 The initial slopes, αr,ofgrowth rate on light intensity from Fig. 5.4, plotted against the corresponding values of msv−1, the product of maximum dimension and the surface-to-volume ratio, of each of the same selection of species of algae: Ana, Anabaena flos-aquae; Aphan, Aphanizomenon flos-aquae; Coel, Coelastrum microporum; Dict, Dictyosphaerium pulchellum; Fra b, Fragilaria bidens; Lim red, Limnothrix redekei; Mic, Microcystis aeruginosa; Monor, Figure 5.4 Light dependence of growth rate at 20 ◦C, as a Monoraphidium sp.; Ped b, Pediastrum boryanum; Pla ag, function of intensity, in a selection of freshwater Planktothrix agardhii; Scen q, Scenedesmus quadricauda. The α = phytoplanktic species. The algae are: Ana, Anabaena flos-aquae; least-squares regression fitted to the points is r 0.257 −1 0.236 Aphan, Aphanizomenon flos-aquae; Coel, Coelastrum microporum; (msv ) . Redrawn with permission from Reynolds Dict, Dictyosphaerium pulchellum; Fra b, Fragilaria bidens; Lim (1997a). red, Limnothrix redekei; Mic, Microcystis aeruginosa; Monor, Monoraphidium sp.; Ped b, Pediastrum boryanum; Pla ag, Planktothrix agardhii; Scen q, Scenedesmus quadricauda. light antennae, at least when oriented correctly Redrawn with permission from Reynolds (1997a). in the photon-flux field. The filamentous arrangement cells in the Oscillatoriales seems to be supremely efficient in this context, as both the flux density, which does, eventually, force a numerous studies referred to above and the affin- dependence of r on I. The steeper is the slope of ity the Planktothrix and Limnothrix species for tur- light-dependent growth (αr), the more efficient bid, well-mixed lakes (see Section 7.2.3)would is the dedication of harvested light energy. Val- indicate. Recalculating from the data of Post et ues of αr (expressed in units of specific replica- al.(1985), acclimated P. agardhii may maintain a tion rate (r)d−1 (mol photon)−1 m−2 per d, which maximum growth rate of 9.8 × 10−6 mol C (mol simplifies to (mol photon)−1 m2), are derived cell C)−1 s−1 at 20 ◦C, to as low as 18 µmol pho- −2 −1 −1 from the initial, light-dependent slopes in Fig. tons m s ; αr ≈ 0.54 mol C (mol cell C) (mol 5.4.Following Reynolds (1989b), they are plot- photon)−1 m2. The analogous experimental data ted inFig.5.5 against the dimensionless prod- forthe diatom Asterionella have not been located uct of the surface-to-volume ratio (sv−1)andthe but, piecing together information from field pop- maximum dimension of the alga (m). This had ulations, Reynolds (1994a)showedittorivalthe been found to provide the most satisfactory mor- reputation of Planktothrix as a low-light adapting = phological descriptor of the interspecific variabil- organism. From a specific growth rate, r20 20.6 −6 −1 −1 ity in αr.Italsocorresponded with the inter- × 10 mol C (mol cell C) s and a chlorophyll pretation that the greatest flexibility of algae to content of 2.3 pg cell−1,that is ∼0.324 g chla (mol enhance their light-dependent growth efficiency cell C)−1,the sustaining chlorophyll-specific yield evidently resided with those having the great- is 63.6 × 10−6 mol C (g chla)−1 s−1.Inturn,this est morphological attenuation of form. Ostensi- requires a photon flux of, theoretically, not less bly, slender and flattened shapes make the best than 509 × 10−6 mol photons (g chla)−1 s−1 and 192 GROWTH AND REPLICATION OF PHYTOPLANKTON

∼700 × 10−6 mol photons (g chla)−1 s−1,onthe but these are not followed here. In a turbid envi- best performances measured by Bannister and ronment, much of the light available for intercep- Weidemann (1984). The maximum area projected tion is already scattered and at these low aver- by a single Asterionella cell is approximately 200 age intensities, changes of orientation prove to × 10−12 m2 or, with this chlorophyll content, 87 be of little consequence. Well-distributed light- m2 (g chla)−1. The requisite active photon flux is harvesting complexes are everything. calculable as 700 × 10−6 mol photons per 87 m2, These considerations emphasise the influen- or just 8 µmol photons m−2 s−1. This assumes tial nature of the relationship between algal all wavelengths of visible light are utilised but, if shape in the interception of light energy and the only half were usable, the growth-saturating light impact of algal size in governing its metabolism. intensity would be similar to the level measured Morel and Bricaud (1981)recognised this rela- for Planktothrix agardhii. tionship some years ago, referring to the ‘pack- It is not, at first sight, at all obvious that aging’ effect on pigment deployment (cf. Duy- low-light adaptation should be related to algal sens, 1956), where the area projected by the morphology when it is functionally dependent pigments assumed the same relevance as the upon appropriate enhancements in pigmenta- concentration of LHC receptors. It is thus inex- tion. However, it is easily demonstrated that cell tricably linked to the contestable size allome- geometry and orientation raise the efficiency of try of growth rate (with its −1/3slope instead light interception by the pigment complement of the expected −1/4; see Section 5.3.1 above (Kirk, 1975a, b, 1976). A spherical cell, d µmin and Finkel, 2001). A general relationship between diameter, has a volume, v = 4/3π (d/2)3, while the projection and morphometry is shown in Fig. area that it projects is that of the equivalent disc, 3.12. The independent variable is, again, the − a = π(d/2)2.Because the carbon content is, pri- index msv 1,the product of the maximum marily, a function of volume, the carbon-specific cell dimension (m) and the surface-to-volume projection (ka)ofsphericalalgae diminishes with ratio. Note that it is a dimensionless prop- increasing diameter. For example, we may calcu- erty, length always cancelling out. For spheres, − late that, for a single cell of Chlorella (a = 12.6 × m = d,andmsv 1 is a constant [d × 4π(d/2)2 −12 2 −12 ÷ / π / 3 = 10 m ;Ccontent = 0.61 × 10 mol C), ka = 4 3 (d 2) 6]. For any shape representing − 20.7 m2 (mol cell C)−1;foraspherical Microcystis distortion from the spherical form, msv 1 > 6. colony (d = 200 µm), comprising 12 000 cells, Figure 3.12 also shows that the smaller algae each containing 14 pg C (Reynolds and Jaworski, generally project large carbon-specific areas but 1978), in which a = 31.4 × 10−9 m2 for a content larger ones have to be significantly subspherical −9 2 −1 of 14 × 10 mol C, ka = 2.24 m (mol cell C) . to match the ka values of the smaller ones. It is In the case of non-spherical algae that are flat- especially interesting to observe that the algae tened in one, like those of Pediastrum,orintwo that already project the greatest area in relation planes, likethoseofClosterium, Synedra or Asteri- to their cell-carbon content are also mostly those onella,thearea projected depends upon orienta- with the maximum photoadaptive potential. tion. The maximum area projected is when the two longest axes are perpendicular to a unidirec- 5.4.2 The effect of persistent low tional photon source. The typical cell of Asteri- light intensities onella in a colony lying flat on a microscope Rather than experiencing alternations of dark slide is ∼65 µminlengthandshowsatapering interludes with windows of saturating light, phy- valve withanaveragewidth of ∼3.3 µm. In rela- toplankton of so-called crepuscular habitats are tion to its approximate carbon content of 85 pg exposed to variability that offers only windows of (7.08 × 10−12 mol C;Reynolds, 1984a), the maxi- gloom. The algae forming metalimnetic swarms 2 −1 mum value of ka is ∼ 28.2 m (mol cell C) .In and deep chlorophyll maxima (DCM) in stable lay- other orientations relative to a single source of ers in seas and lakes experience the same circa- light, the area projected may greatly diminish. dian alternations of night and day perceived by Kirk’s (1976) calculations compensated for this terrestrial and littoral plants but, because they REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 193 are located so relatively deep in the light gradi- (Ganf et al., 1991). Taking as the most extreme ent, the daytime irradiances they experience are case of photosynthetic efficiency from Post et al. low. (1985)forP. agardhii as a proven example of the The circumstances of a cell placed at a con- low-light adaptation that is possible at 20 ◦C (viz. stant depth and receiving a dielly fluctuating 0.54 mol C (mol cell C)−1 (mol photon)−1 m2; Sec- but low-intensity insolation differ from those tion 5.4.1)andcomparing it with the supposed of one receiving short bursts of high illumina- basal rate of respiration of an alga of its dimen- tion, even though the daily photon flux might sions, 0.079 (s/v)0.325,i.e.∼0.064 mol C (mol cell be similar. However, the ultimate objective – to C) d−1,or0.74 ×10−6 mol C (mol cell C)−1 s−1 maximise absorption of the photons available at the same temperature, it is possible to deduce – does invoke certain similarities of response. that compensation is achieved at ∼1.4 µmol pho- All the organisms that successfully exploit sta- tons m−2 s−1,certainlyinthe order of 3–4 µmol ble layers have to be capable of maintaining ver- photons m−2 s−1,ifallowanceforthedark period tical position with respect to the light gradient. is accommodated. They are either motile (e.g. the flagellated chrysophytes that form layers in oligotrophic, soft- 5.4.3 The effect of fluctuating light water lakes and certain species of cryptophyte Applying the results of laboratory experiments of slightly more enriched lakes), or they regu- to the extrapolation of field conditions or to late buoyancy (as do some of the solitary filamen- theinterpetation of field data requires caution. tous Cyanobacteria, including, most familiarly, In the context of the growth responses of phy- Planktothrix rubescens and other members of the toplankton entrained in mixed layer, insolation prolifica group of species, and Planktolyngbya lim- may change rapidly, either increasing or decreas- netica). Buoyancy-regulating sulphur bacteria of ing at random (Fig. 3.14). Depending on the light the Chromatiaceae and Chlorobiaceae may strat- gradient and on the depth of turbulent entrain- ify in the oxygen gradient, provided this lies ment, phytoplankters might experience anything simultaneously within a stable density gradient from a probable period of 30–40 minutes in effec- and is also reached by a few downwelling pho- tive darkness with a few minutes of exposure tons (usually ≤5 µmol m−2 s−1). Here, photoau- to high light (deep mixing, steep light gradient), totrophs function on inputs of light energy that to asimilar time period of fluctuating light lev- are invariably low. The extent of photoadaptation els that are nevertheless adequate to support net demanded of them depends essentially upon the photosynthesis throughout (mixing within the depth in the light gradient at which the organ- photic zone). The generic nature of the adaptive ism is poised. This determines the quantity of responses available, discussed here and in Section penetrating irradiance and the wavelengths of 3.3.3,isclearly aimed towards optimising growth theresidual light least absorbed at lesser depths against highly erratic drivers. However, the prob- (the quality of the irradiance). Beneath relatively abilistic, Eulerian aggregation of the responses clear layers, with absorption predominantly in of the whole population does not take account theblue wavelengths, the pigmentation may be of the photoprotective and recovery behaviour expected to intensify but without obvious chro- on the growth rates of individual cells to what matic adaptation. The less is the residual light in are sometimes sharp, sudden and possibly cru- the red wavelengths, however, the more advan- cial changes in insolation. tageous is the facultative production of acces- There are experimental data that lend per- sory pigments, such as phycoerythrin and phy- spective to this issue. Litchman (2000)designed cocyanin, to the organism’s ability to function experiments that brought irradiance fluctuations phototrophically at depth. to each of four cultured microalgae, in each As discussed in Section 3.3.3,the adaptation of three ranges (15–35, 15–85 and 65–135 µmol is most plainly observed in depth-zonated popula- m−2 s−1)and over three wavelengths of fluctuations of Cyanobacteria (Reynolds et al., 1983a)or tion (1, 8 and 24 h). Variations in the low-light in populations slowly sinking to greater depths range (15–35 µmol m−2 s−1, wherein growth rate 194 GROWTH AND REPLICATION OF PHYTOPLANKTON

is expected to be proportional) were fairly neu- circumstances, able to take up nutrients far faster tral. The growth rate of the diatom Nitzschia was than they can deploy them. Moreover, they can slightly increased, that of the green alga Sphaero- continue to do so until very low resource con- cystis schroeteri wasslightly depressed, compared centrations are encountered. Even then, the lux- to growth at a constant 20 µmol m−2 s−1.Inthe ury uptake in generations experiencing resource saturating range (65–135 µmol m−2 s−1), little plenitude may support two or three generations effect was experienced, except that Anabaena flos- born to resource deficiency. aquae wasslightly increased over its performance At first sight, there is certainly a rapid tran- at a steady 100 µmol m−2 s−1.Overthe wide sition from there being no competition for range of fluctuations (15–85 µmol m−2 s−1,span- resources to there being little left over which ning limitation to saturation), growth responses to compete. There is a counter to this deduc- differed significantly from the behaviour under tion, which refers back to the distinctions in the steady exposure. Growth of all species was main- strategies of velocity, storage and affinity adapta- tained on the short (1-h) cycle; in each case, the tion (Section 4.3.2). Naturally, fast-growing algae relatively short exposure to high light remained must be able to garner resources with equal within the capacity of the species-specific phys- velocity, from diminishing external concentra- iologies. On the longer cycles, however, growth tions. To be able to store resources in excess rate wasimpaired in all species, though not all promises an advantage when external concentra- to thesame extent. The reaction would once tions have been diminished, although it might be have been described as ‘photoinhibition’ but more beneficial to species that have the ability to would now be better referred to photoprotection migrate between the relative resource-richness of and the first steps toward photoadaptation (see deep-water layers and resource-depleted but inso- Section 3.3.4). The experiments of Floder¨ et al. lated surface waters. To survive, even to thrive, in (2002)investigated the influence of fluctuating waters chronically deficient in one (rarely more) light intensities (range 20–100 µmol m−2 s−1) major resource might well call for a superior on growth rates of natural phytoplankton assem- competitive ability to win the scarce supplies and blages collected from Biwa-Ko, imposed on cycles deny them to individuals of other species. of 1, 3, 6 or 12 days. These ably illustrate the Evidence for the existence and implementa- population responses consequential upon differ- tion of these strategies is to be discussed later in ential growth rates altering the composition of this chapter. For the moment, the first task is to the assemblage. discern the resource levels that separate famine from bounty. It is convenient to consider these 5.4.4 The effects of nutrient deficiency nutrient by nutrient. A cornerstone role has long been accorded to nutrients in the regulation of productive capac- Phosphorus deficiency ity in the plankton and in shaping the species Satisfaction of the alga-specific P requirements composition. A very large literature on the nutri- forgrowth has been suggested to rest upon the ent limitation of phytoplankton and the inter- ability to maintain a stoichiometric balance of specific competition for resources reflects the assimilates approximating to 1 P atom to every importance of their availability in pelagic ecol- 106 of carbon. This determines the generalised ogy, even if these key processes seem, at times, requirement that 9.4 × 10−3 mol P (mol C)−1 is to have been misrepresented. The point has been incorporated during each single replication time. made earlier that the least-available resource, rel- As already indicated, the alga’s uptake capacity is ative to the minimum requirements of organ- likely to be such that, under resource-rich condi- isms, sets a finite ‘carrying capacity’ for the habi- tions, it may achieve this in minutes rather than tat. To establish the limiting role of nutrients on hours. It is not likely that any phytoplankter takes growth rate is more difficult, for two reasons. As longer than its achievable generation time while has been shown in Chapter 4 and again in Sec- external MRP concentrations exceed 0.13 × 10−6 tion 5.3.3,most phytoplankters are, under ideal M(4µgPL−1). For many species, indeed, this REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 195 could be true at MRP concentrations as low as (Section 4.3.2), found that growth rate at 20 ◦Cis 10−8 M (0.3 µgPL−1;seeSections 4.3.3, 5.3.3). half-saturated when the cell contains about 0.7 Even then, the reserves accumulated during pre- pg P (or about 0.003 mol cell P (mol cell C)−1). vious resource-replete generations may sustain The external MRP concentration required to bal- −1 one or two generations before the cell recog- ance this quota is about 0.75 µgPL (Kr = 0.024 nises impending shortages and perhaps three, µM). The extensive work of Tilman and Kilham or even four, before the cell quotas approach (1976) using semi-continuous cultures of diatoms q0 and exhaustion. Fast-growing species, having pointed to the half saturation of growth in Asteri- high sv−1 (>1.3 µm−1, which, at about 30 ◦C, onella formosa falling between 0.02 and 0.04 µmol might permit specific growth rates of up to ∼4 PL−1 (0.6–1.2 µgPL−1). However, the correspond- d−1,or∼50 × 10−6 s−1,tobeattained), would ing value for another diatom, Cyclotella menegh- be expected to reach exhaustion proportinately iniana,was substantially higher than this (Kr = sooner. Yet averaging and normalising the total 0.25 µmol P L−1,ornearly8µgPL−1). Finally, in Prequirements to the starting biomass carbon, this context, Nalewajko and Lean (1978)used32P- the P demand of two generations (∼0.5 × 10−6 labelled phosphorus to track phosphorus uptake mol P (mol initial cell C)−1 s−1)isstilllikelyto and turnover in cultures of Anabaena flos-aquae be deliverable from a starting concentration of and Scenedesmus quadricauda,and remarked on 0.03–0.13 × 10−6 M (1–4 µgPL−1). the‘low’ concentrations (∼6 µgPL−1; ∼0.2 µmol Data compilations that compare growth rates, PL−1)atwhich full exchange activity is main- nutrient-uptake rates and their half-saturation tained. coefficients are available (see Padisak,´ 2003), from Certainly, most of these data uphold the view which it ought to be a straightforward exer- that the onset of phosphorus ‘famine’, below cise to verify, on the basis of hard, experimental which growth rate may be regulated by the sup- results, some of the above conjectures. The trou- ply of P, generally occurs at <0.1 µMP(∼3 ble is that many of the half-saturation concen- µgPL−1). This may not apply to all species: trations refer to uptake by starved cells, rather Scenedesmus and the Cyclotella of Tilman and Kil- than to that needed to half-saturate the require- ham are possible exceptions. For most species, ment tomaintain growth (Kr). These quantities allusions to growth-rate limitation of phytoplank- require the analysis of a lot of batch cultures, ton byphosphorus when external MRP concentra- across a range of concentrations, or the appli- tions exceed 0.1 µMPmay be doubted. It is pos- cation of a semi-continuous technique in which sible that the higher species-specific thresholds the algal culture is diluted with test medium are a consequence of adaptation to the relatively at a rate adjusted to keep the algal concen- P-rich habitats in which they occur. Conversely, tration constant (that is, to balance the rate differential species-specific affinities uptake (Kr of growth). As a consequence, there are few values spanning 0.01–0.2 µMP)can be said to good data to confirm the half-saturation con- influence where species may live and how com- stants of P-limited growth. Rhee (1973), using a petitive they might be for truly limiting supplies Scenedesmus, Ahlgren (1985), with Microcystis wesen- of phosphorus. bergii,andSpijkerman and Coesel (1996a), using two desmids (Cosmarium abbreviatum and Stauras- Nitrogen deficiency trum pingue), each found that the algae would Analogous calculations concerning algae and grow at about one half the nutrient-saturated their nitrogen requirements are also available. rate at 20 ◦C, in media supplying <6.0 µgPL−1 Supposing the satisfaction of the alga-specific N (0.19 µM). All but the Scenedesmus did so at requirements for growth to be similarly based <1.2 µgPL−1 (<0.04 µM). Cosmarium growth upon the stoichiometric balancing against car- rate was half-saturated at 0.35 µgPL−1 (0.011 bon in the atomic ratio 6.6 : 1, the generalised µM). Davies (1997), whose work with Asterionella demand approximates to 151 × 10−3 molN(mol has been highlighted earlier in the context of C)−1.Again the DIN-uptake capacity is well up theinteraction between P-uptake and cell quota to this under nitrogen-replete conditions. From 196 GROWTH AND REPLICATION OF PHYTOPLANKTON

the information on DIN uptake in Chlorella (Sec- imprecise. In many of the nitrogen-deficient but tion 5.3.3), it may be deduced that the nitrogen simultaneously phosphorus-poor lakes of the complement needed to sustain a doubling of Andean–Patagonian lakes investigated by Diaz mass could proceed 60 times more slowly and and Pedrozo (1996), the phytoplankton biomass still fulfil the maximum growth rate. Moreover, is demonstrably (by assays and by mathematical the external concentration needed to supply DIN regession) constrained by nitrogen availability. at this rate would be about 0.12 µmol N L−1, The significant incidence of dinitrogen-fixing or 2 µgNL−1). The half-saturation constants Cyanobacteria is relatively restricted to lakes, for nitrate and ammonium uptake (KU)among such as Bayley-Willis and Fonck, that have higher small-celled oceanic phytoplankton are of simi- TP contents (and where, incidentally, the SRP is lar order or only slightly higher (see Section 4.4.2) drawn down in summer to growth-limiting levels and are, thus, unlikely to experience symptoms as identied above, viz. to <0.1 µM P). Elsewhere, of nitrogen-limited growth at external DIN con- the unsupplemented combined levels of nitrate-, centrations >1–2 µgNL−1.Ontheother hand, nitrite- and ammonium- nitrogen levels stand at the half-saturation constants for nitrate and ≤0.8–1.0 µM(≤11–14 µgNL−1), perhaps falling ammonium uptake (KU)amonglarger diatoms of in summer to <0.2 µM(seeDiaz et al., 2000). inshore waters may be up to an order greater The revised verdict on the DIN levels repre- again (0.5–5 µM N), so that problems of obtaining senting the onset of nitrogen limitation among sufficient nitrogen to even half-saturate growth non-fixers is 0.1 µM(1.5µgNL−1)foroceanic might be experienced at external DIN concentra- picoplankton and 1–2 µM(15–30 µgNL−1)for tions in the range 0.2–2 µMN(say 3–30 µgN many microplankters in lakes and seas. If other L−1). conditions are satisfied (see Section 4.4.3), nitro- The lower limits of the range of DIN concen- genfixers may avoid altogether the constraint of trations able to support phytoplankton growth low DIN concentrations. in inland waters are less well researched. It was once deduced (Reynolds, 1972)that, based on Silicon deficiency the assumption that the appearance of nitrogen- Silicon limitation of growth in diatoms is abso- fixing organelles (nostocalean heterocysts) at DIN lute and well understood. Lund’s (1949, 1950)clas- levels of 20–25 µMprovided a simultaneous sical studies on Asterionella in Windermere and advantage to the fixers over non-fixers, the non- its relationship with the availability of silicon fixers were experiencing supply difficulties. As helped to establish the importance of nutrients aresult of later observations but without vary- in planktic ecology. The clarity of the effects ing the essential logic, this critical range was and the precision of the chemical thresholds revised downwards to ∼6–7 µMN(80–100 µgN were, and are still, impressive. That they were L−1)(Reynolds, 1986b). As it now seems probable never emulated in the studies of other elemen- that heterocyst production responds to ammonia tal requirements is attributable to the nature of concentration and not DIN per se (discussion, sec- the nutrients and the margin around the empiri- tion 4.4.3), it no longer follows that their appear- cism of the requirements that the organisms ance necessarily coincides with nitrogen shortage introduce through storage and luxury uptake. As among the nitrate users. Current evidence indi- stated (Section 4.6), the diatoms are the biggest cates that they are competent to draw down DIN planktic consumers of silicon; they take up no to concentrations to levels of 0.3–3 µMwithout more than is required to build the silica valves growth-rate limitation. of the frustules of the current generation, and Eventually, the ability of heterocystous thesilicon polymer is laid down under close cyanobacteria to fix nitrogen when DIN is simul- genetic supervision. All this leads to the sili- taneously depleted influences the recruitment of con requirement of each new cell of a given to natural communities (Riddolls, 1985)butthe species and size being readily predictable. The concentration threshold favouring Cyanobacte- concentrations of silicic acid capable of deliv- rial dominance, between 2 and 6 µMN,remains ering the silica requirement have been found REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 197 through observation and experiment. The conse- established an important conceptual theory of quence of silicon ‘limitation’ is easy to detect as resource-based competition.Simply, if two species, A its consequence is that cells cannot complete the and B, having similar resource-saturated growth growth cycle. Moreover, failure of the putative rates, are cultured together in a gradient of cell to build its new frustular valve is fatal. growth-limiting concentrations of a resource S1, In the case of Lund’s Asterionella,theaverage theone with the higher uptake rate (VU)isclearly −1 complement of 140 pg (SiO2)n cell could be sat- able to sustain a faster rate of growth at low con- isfied from a concentration equivalent to ≥0.5 centrations of [S1]thantheother.The theoretical −1 mg (SiO2)L .Translation of the units notwith- growth performances of A and B are shown in standing, both quantities have been abundantly Fig. 5.6a. Against a second resource, S2,however, verified. Solving the regressions of Jaworski et al. it is species B that performs better at low concen- (1988), an Asterionella cell 65 µminlengthhas trations (Fig. 5.6b). Placed together in a medium −1 aprobable Si content of 65 pg (2.3 pmol cell ). deficient in both S1 and S2,itispossible, depend- Using the experimental data of Tilman and Kil- ing on the relative concentrations of either nutri- ham (1976), the silicic acid concentration that ent, for the species to be simultaneously lim- will half-saturate the Si requirement is 3.9 µM ited by different nutrients. Plotting against the −1 (equivalent to 109 µgSiL ,or0.23 mg (SiO2)n concentrations of both resources (Fig. 5.6c), the L−1). respective limitations can be used to predict com- Equivalent data from many other experi- petitive outcomes of variable resource combi- ments, reviewed in Tilman et al.(1982)and nations (Fig. 5.6d). Thus, at low concentrations in Sommer (1988a), show that growth rates of of (S1), an outcome will always be favoured in freshwater diatoms at 20 ◦Ctendtobehalf- which A dominates; at low concentrations of saturated at between 0.9 (in Stephanodiscus min- ions of (S2), it will be B that is favoured. At utus)and20µMSi(inSynedra filiformis). That slightly higher concentrations of both resources, of Cyclotella meneghiniana is half-saturated at 1.4 Aand B may coexist successfully, while the µMSi(Tilmanand Kilham, 1976). Among the one (B) remains S1-limited and the other is investigated clones of marine Thalassiosira pseudo- still limited by S2. This prediction was pre- nana and T. nordenskioeldii, half-saturation of the cisely the outcome of their investigations (Tilman growth rate at 20 ◦Ctends to occur in the range and Kilham, 1976)ofphosphorus- and silicon- 0.2 to 1.5 µM (data of Paasche, 1973a, b). limited growth between Asterionella formosa −1 The 100-fold range in uptake thresholds has (Kr(P), ∼0.03 µmol P L , Kr (Si) 3.9 µmol Si −1 ecological consequences, to be considered in the L )andCyclotella meneghiniana (Kr(P), ∼0.25 µmol −1 −1 next section.For the moment, the deduction PL , Kr (Si) 1.4 µmol SiL ); Cyclotella domi- is that silicon concentrations begin to interfere nated over Asterionella in mixed cultures at low with the growth of diatoms at concentrations Si : P ratios. The opposite was true at high Si : P below ∼0.5 mg Si L−1 (say 1mgL−1 as equivalent ratios. On the basis of later investigations of silica, or ∼20 µM). In most lacustrine instances, other species, Tilman et al.(1982)emphasised the growth-limiting concentrations are encountered differential competitive abilities of diatoms to −1 mainly below about 0.1 mg Si L (say <4 µM) Si:Pbyplotting the experimentally solved Kr(P) −1 and, in the sea, below 0.03 mg Si L (<2 µM). against Kr(Si) for each (see Fig. 5.6e). The plot ably arranges species on the basis of Si:Ppreferences. 5.4.5 The effect of resource interactions: For most other plankton, silicon is a minor nutrients and light nutrient and, not surprisingly, they tolerate Si:P Resource-based competition ratios very much lower than Cyclotella’s limit The able demonstrations by Tilman and his co- of 5.6 (Holm and Armstrong, 1981; Sommer, workers of the interspecific differences in the 1989). However, it is the relationships between capability of diatoms to take up the silicon thenitrogen and phosphorus requirements that and phosphorus required to sustain their growth have aroused enormous interest, especially in the from relatively low external concentrations also context of a widely held belief that low 198 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.6 Resource competition and species interactions. Parts (a) and (b) compare the nutrient-limited growth rates two species of phytoplankter, Sp. A and Sp. B, against low, steady-state concentrations of resources S1 and S2.Growth of either may be limited (c) by the availability of either resource. Tilman’s theory of resource-based interspecific competition acknowledges that the uptake constraints acting on Sp. A and Sp. B differ sufficiently for (d) Sp. A to dominate over Sp. B when [S1]islowandSp.B to do so when [S1]islow, but Spp. A and B do not compete when limited by different resources. The relative competitive abilities of named diatoms for silicate and phosphate, as determined by Tilman et al.(1982), are shown in (e): A.f., Asterionella formosa; C.m., Cyclotella meneghiniana; D.e., Diatoma elongatum; F.c ., Fragilaria crotonensis; S.f., Synedra filiformis; S.m., Stephanodiscus minutulus; T.f., Tabellaria flocculosa.In(f), the effects on phytoplankton assemblages in a selection of natural lakes of differing N and P availabilities are represented: C, Crose Mere, and W; Windermere, are in UK; E is Esrum, Denmark; K, Kasumiga-Ura, and S, Sagami-Ko, Japan; Me, Mendota, T, Tahoe, and Wa, Washington, in USA; Mg is Maggiore, Italy/Swizerland and Ml, Mälaren, in Sweden. Area 1 applies to low-P lakes, dominated by diatoms and chrysophytes; area 2 covers lakes in which nitrogen-fixing Cyanobacteria are abundant through substantial parts of the year; area 3 lakes are are dominated by Microcystis for long periods. The composite combines figures redrawn from Reynolds (1984a) and Reynolds (1987b).

nitrogen-to-phosphorus ratios favour the (usually ing normal growth (when both storage effects unwelcome) dominance of Cyanobacteria (Smith, and deficiencies should have been minimal). Out- 1983). Rhee (1978)suggested that the evident comes ranged between 7, for the diatom Stephano- mutual competition along N : P gradients is influ- discus binderanus, and 20–30, for three species of enced by differing N : P optima in the cells Chlorococcales. For the Cyanobacterium Microcys- of various species. In a major programme of tis aeruginosa,itwas 9. These optima differ from laboratory experimentation, Rhee and Gotham theideal (‘Redfield’) N : P stoichiometry centred (1980)showedsystematic differences in the ratios at 16 molecular and from the suggested (Section of species-specific optimal N and P quotas dur- 4.4)rangeof normality of 13–19. Given the range REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 199 in physiological variability in N : C and P : C con- Stoichiometry tent of individual cells, extremes of N : P of 4 and These plausible deductions invoked parallel 108 are theoretically tenable but values within developments in the appreciation of organismic therange 10 to 30 are scarcely indicative of nutri- stoichiometry, prompted, in part, by the work of ent stress. Hessen and Lyche (1991)onthedifferential ele- Nevertheless, the findings of Rhee and mental make up (chiefly C:N:P) of zooplankton. Gotham (1980)donotviolate any supposition Stoichiometric differences between the trophic about the importance of N : P ratios in favour- components imply consequences for the system ing Cyanobacteria or otherwise. However, there as a whole. For instance, animals with a relatively are difficulties (see below) in applying resource low N : P content feeding on algal foods having ratios to either the interpretation or the pre- ahighN:Pmake-up will retain P preferentially diction of the composition of natural communi- and, so, recycle wastes with a yet higher N:P con- ties. Besides, ratios of available resources change tent. This approach has been developed further quite rapidly through time, without necessarily by J. Elser and co-workers (usefully reviewed in precipitating immediate changes in species com- Elser et al., 2000). They were able to demonstrate position. If the total nitrogen and phosphorus striking connectivities among the molecular sto- resources delivered to and present within a water ichiometries of growing cells of a wide range body are considered, some broad compositional of algal species, their rates of growth and the trends are discernible. The distribution of lakes evolutionary pressures underpinning their life- shown inFig.5.6fagainstaxesof total N and history traits. That is to say, the evolution of fast total P separates those that will support large or slow growth rates and the allocation of the populations of nitrogen-fixing Cyanobacteria as catalysing (P-rich) RNA molecules are inextricably being low-N-high-P habitats, from those that sup- interlinked. The matching of evolutionary traits, port non-fixing Microcystis (high N, high P) and from their molecular bases to the environments those that seem never to be dominated by bloom- in which whole organisms function and interact, forming genera (low-P lakes). now has a wide following. The recent book by To be any more specific about predictions of Sterner and Elser (2002)onEcological Stoichiometry differentiated growth or the composition of the conveys and nourishes much of this excitement. population structures that it might yield needs Besides providing an alternative perspective on much more information. One component obvi- ecosystem function and a persuasive argument ously lacking from the previous paragraph is the forunifying concepts in its understanding, the carbon input and the solar-energy income that book invokes pertinent explorations of just what is essential to its compounding with nutrient goes on inside the living cell to yield recognisable resources into biomass. In developing a hypoth- structural stoichiometries in the first place and esis about the deterministic importance of the what activities lead to (relatively modest) depar- light : nutrient ratio in lakes, Sterner et al.(1997) tures therefrom. showed that the relationship between the mean To bring us back specifically to phytoplank- mixed-layer light level (equivalent to the calcu- ton, if these attractive theories of resource ratios lation of I∗ in Section 3.3.3)ineach of a num- and biological stoichiometry are to be helpful to ber of lakes and its corresponding total P con- understanding how pelagic communities func- centration is a good probabilistic predictor of tion, then it is important first to separate just the C:Pcontentofthesestonandoftheeffi- what is cause and what is effect. It is necessary ciency of resource use by the system as a whole. to emphasise the distinctions among the ratios They further hypothesised that the seston C : P of algal cell quotas, the ratios of resource avail- ratio influenced the pathways of secondary pro- ability and supply, and the competitive abilities duction (essentially the food-web consumers of of algae to take up elements at low concentra- primary product) and thence, biassed the intentions. Taking cell quotas first, we have to accept sity of nutrient recycling, the strength of micro- that the ratio N : P = 16 is certainly not abso- bial processing and, indeed, the structuring of lute, that it is subject to a margin of physiological the entire ecosystem. variability, including in the complement of RNA, 200 GROWTH AND REPLICATION OF PHYTOPLANKTON

and that there may indeed be systematic, inter- and a probable biomass N : P (5.3) indicative phyletic differences in the optimal elemental bal- of N-limitation. The residual P concentration ances. Nevertheless, the range of normality in the (arguably ∼0.7 µmol P L−1) confirms that P is elemental composition of cells, from bacteria to certainly not a constraint and it is also suffi- elephants, is relatively quite narrow, reflecting cient to support the activity of nitrogen-fixing general similarities in the cell complements of Cyanobacteria. These could grow to the limit protein and nucleic acid (Geider and La Roche, of the phosphorus capacity (47 µgchla L−1), 2000). From Chapter 4,itisplainthat a factor of only to now be dominated by nitrogen-fixing 50% variation in either the N or the P content is Cyanobacteria having an intracellular N : P ratio hardly exceptional, yet it yields a full range in N:P of ∼30. Note that, provided it is not itself from 5 to 36. For the purpose of estimating stoi- limited by some other factor, nitrogen fixa- chiometrically the phytoplankton-carrying capac- tion forces the nitrogen-deficient system to the ity of the nutrients in a given habitat, less error capacity of its phosphorus supply (cf. Schindler, attaches to the adoption of a mean complement 1977). of 16 to 1 than to the correct estimation of the baseofbioavailable nutrients (Reynolds and Resource depletion and growth-rate regulation Maberly, 2002). However, it is more straightfor- Now let us consider the role of interspecific com- ward (and more illuminating) to examine the petition in the way different species might simul- support resource by resource. To be able to form taneously satisfy their resource requirements to astandingphytoplankton biomass equivalent to, sustain their growth rates. Here we bring into say, 106 µmolCL−1 (1.27 mg C L−1, ∼25 µgchla sharp focus the uptake capabilities of the algae L−1)ostensibly requires the supply of 16 µmol N themselves and the sorts of threshold concentra- and 1 µmol P L−1 (i.e. 224 µgN,31µgPL−1). If tions at which they fail to be able to take up the water body can fulfil only 10 µmol N and 0.1 specific nutrients as fast as maximum consump- µmolPL−1 (note, N : P = 100), it is obvious that tion would demand (1–2 µmol N, 0.1 µmol P thegrowth demand will first exhaust the phos- L−1 (Section 5.4.4). The corollary of this is that phorus, at a rather smaller chlorophyll yield than if the concentrations of bioavailable N and P 25 µgchla L−1. Long before this maximum is are significantly greater than these thresholds, reached, the biomass : P yield is stretched, accord- neither imposes a rate-limiting constraint upon ing toEq.(4.15), to 12.2 µgchla L−1;thebiomass thegrowth of any alga. Several species could has a probable content of carbon equivalent to grow simultaneously and, while each satisfies its ∼51 µmolCand7.7µmol N L−1,butnomore requirement, they are not in mutual direct com- than the originally available 0.1 µmolPL−1.We petition (sensu Keddy, 2001;seeBox4.1). Each per- deduce a biomass N : P ratio of 77, correctly infer- formstoits capacity (or to some independent ring the obviously severe phosphorus limitation regulation). At this stage, the ratio of the available on the biomass. The magnitude of the eventual resources is quite irrelevant to the regulation of species- P-limited quota constraint on the biomass is pre- specific growth rates. dictable on the basis of the initial phosphorus This deduction arouses persistent controversy. availability. That it was phosphorus, rather than Yetitisreadily verifiable in the laboratory nitrogen, that would impose the eventual limit through the measurement of the early exponen- is implicit in the starting resource ratio. tial increase of a test alga in prepared media Now, if the water body could fulfil 1 µmol offering nutrients in differing mutual ratios Pbutonly 1.6 µmol N L−1 (i.e., 31 µgP,22.4 but at initially saturating concentrations. I am µgNL−1; N:P 1.6), growth would be expected to unaware of any publication that draws attention exhaust the nitrogen, for the production of 32 to this behaviour. However, I am most grateful µmol biomass C L−1 (assuming the minimum C to Dr Catherine Legrand, of the University of :Nratioquoted in Section 4.4) and which, stoi- Kalmar, Sweden, for her permission to reproduce chiometrically, would have a phosphorus content agraph that she presented at the 1999 Meet- equivalent to not less than 0.3 µmol P L−1 ing of the American Society of Limnology and REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 201

of the point I wished to illustrate; however, she does not necessarily share my interpretation.) In nature, phytoplankters inhabit dynamic environments, far removed from the contrived and quasi-steady states of the laboratory, and algal consumption will, in many instances, take one or another of the free resources to below the concentration representing its competitive thresholds. It is within this region of potential growth-rate limitation, that Tilman-type resource-based competition is expected to be strongly expressed. Thus, with external concentrations of (say) MRP falling to below 0.1 µmol PL−1, Asterionella may maintain a rate of replication close to the maximum that the temperature and photoperiod may allow, yet Cyclotella, once its reserves are depleted, is able to maintain only a fraction of its resource-saturated growth rate.Given initial parity, its abundance relative to Asterionella is set to fall quickly behind. As the MRP concentration falls yet further, Cyclotella may cease to increase at all, while Asterionella Figure 5.7 Initial increase in cell populations of Alexandrium tamarense KAC01 in laboratory cultures artificial is still absorbing phosphorus that is now effec- media with widely differing ratios ofN:P:ν – 160; – 16; λ – tively denied to the ‘outcompeted’ Cyclotella.Very 1.6. Original data of Dr C. Legrand, replotted with soon, of course, the MRP is too depeleted to permission. See text for further details. be able to support further growth of Asterionella either, and the performance failure is still more abrupt. All this is predicted by the species-specific growth-rate dependence on P concentration Oceanography, held in Santa Fé, NM, USA. Her (Fig. 5.6). paper was concerned with the development of Against gradients of falling silicon concentra- toxicity in a laboratory strain (KAC01) of the tion, Cyclotella can continue to absorb silicic acid dinoflagellate Alexandrium tamarense in relation from concentrations already severely constrain- to the nitrogen and phosphorus resources sup- ing Asterionella. The outcome of interspecific com- plied. Replicate treatments were grown in arti- petition betwen other pairs of diatoms may be ficial media, at17± 1 ◦Candsubjecttoa16-h verifiably predicted according to the model of light : 8-h dark cycle, differing only in the con- Tilman et al.(1982). Another, quite separate, illus- centrations at which nitrogen and phosphorus tration of resource competition was described by were supplied. Media contained either 20 µMN Spijkerman and Coesel (1996b). Of three species and 0.75 µMP(i.e., N : P = 160), or 120 µMN of planktic desmid grown in continuous-flow and 7.5 µM(N:P= 16) or 12 µMNand7.5µM cultures under stringent P-limiting conditions, P(N:P= 1.6). The results, summarised in Fig. one – Cosmarium abbreviatum –showedsuperior 5.7,refertotheincreases in cell concentration affinity for phosphorus at low concentrations of algae grown in the three media. They show over the other two (Staurastrum pingue, S. chaeto- clearly that initial growth performances in the ceras), even though these have faster maximum three media were indistinguishable, though, not P-uptake rates. The outcome of competition in surprisingly, they diverged as the experiment pro- mixed chemostat cultures conformed to the pre- gressed. (Note: When Dr Legrand gave her permis- diction that, at concentrations of <0.02 µmol P sion to use her data, it was in her full knowledge L−1, Cosmarium outcompeted the Staurastra but, 202 GROWTH AND REPLICATION OF PHYTOPLANKTON

at higher delivery rates, their faster rates of missa), as well as in progressive changes in the uptake and growth allowed the Staurastra to nutrient resources in the lake, Asterionella has dominate the numbers of Cosmarium.Ifinstead dominated in all but one of those years. Two of low continuous supply, phosphorus was sup- trends over the period have been unmistakable. plied in single daily doses of 0.7 µmol P L−1, One is that the Asterionella maximum, which, in superior uptake rates enabled the Staurastrum all years, has been contained ultimately within species to sequester relatively more of the pulsed the capacity of the silicon availability (∼30 µmol resource supply (velocity/storage then proving Si L−1 (Lund, 1950)has,onaverage,beencom- more advantageous than high affinity). ing earlier each year (by an average of 30 days In none of these cases is the outcome over 40 years). Second, during the same period, attributable to anything other than the abso- the MRP available to phytoplankton at the incep- lute characteristics of the critical resource sup- tion of the annual growth increased from ply to the needs and sequestration abilities of ∼0.1 to almost 1 µmolPL−1. Early in the period, theorganism(s) concerned. In none is the out- Asterionella may have seem well suited to the high come the direct consequence of the ratio of Si : P conditions, although, in reality, its dom- resources available or of the rate at which crit- inance in any individual year also invoked the ical resources are supplied. Thus, at this stage size of the inocula and its ability to grow on low too, it is not the ratio of available resources that deter- daily light doses. By the time of the maximum mines the outcome. The resource ratio is an inter- (and for a substantial period beforehand), MRP pretative convenience in identifying which of two levels were below the limit of detection. As the scarce resources is likely to be, or to become, lake has become more enriched with phospho- limiting and it aids the understanding of simul- rus, the Asterionella has continued to dominate taneous limitation of coexisting species by dif- the early growth stages but it has been able to ferent resources, provided both are below their maintain an accelerating growth rate, all the way respective critical thresholds. When the limiting to the division that finally reduces the silicon to concentrations of both resources are exceeded, concentrations limiting its ability to take it up the interspecific competition for those resources (Reynolds, 1997b). Under these limiting and now is correspondingly diminished, as both satisfy relatively low Si : P conditions, should we not their immediate needs without interference to expect resource competition to alter the outcome theother, and the likeihood of the one excluding of the spring growth? Reynolds’ (1998a)simple the other is minimised. The explicit prediction of model envisaged a typical standing population of coexistence, inserted in the top right-hand cor- Asterionella of 4 × 106 cells L−1 at the time that ner ofFig.5.6d, is correct but the explanation is thesilicon concentration is lowered to the point different from that applying towards the bottom (8 µmol L−1) where its growth rate is increasingly left-hand side. regulated by the rate of silicon uptake. Its next There is a further perplexity over the gen- and possibly last doubling (it might take 4–7 days eral assumption of resource competition among to complete) would require all of the remaining species, which I have aired at length in cer- silicon in the water. At the same time, the sub- tain earlier publications (Reynolds, 1997b, 1998a). dominant Cyclotella,atnomorethan 0.8 × 106 From a comparison of the interannual varia- cells L−1,isexperiencing neither phosphorus nor tions in the dynamics and composition of the silicon limitation and maintains the maximum phytoplankton through successive spring phy- growth rate that the temperature and the light toplankton blooms in Windermere since 1945, regime will allow, as predicted by the Tilman several dynamic characteristics have been recog- model. The difficulty is that before the altered nised (Maberly et al., 1994;Reynoldsand Irish, competitive basis can be expressed at the level of 2000). Despite interannual differences in temper- community composition, the silicon is effectively ature, rainfall and stratification, in the size of exhausted. There is no advantage to better com- theinocula and the rates of growth attained petitors for a non-existent resource: Asterionella by each of several speciesofdiatom(Asterionella still dominates, despite its (by now) competitive formosa, Aulacoseira subarctica and Cyclotella praeter- inadequacies. REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 203

Ta b l e 5.2 Phytoplankters tolerant or indicative of chronically oligotrophic conditions in lakes and the upper mixed layers of tropical oceans

Lakes Cyanobacteria Synechococcoid picoplankton Chlorophyceae Chlorella minutissima, Coenocystis, Coenochloris (Eutetramorus), Sphaerocystis, Oocystis aff. lacustris, Willea wilhelmii, Cosmarium, Staurodesmus Chrysophyceae Chrysolykos, Dinobryon cylindricum, Mallomonas caudata, Uroglena spp. Bacillariophyceae Aulacoseira alpigena, Cyclotella comensis, C. radiosa, C. glomerata, Urosolenia eriensis Sources:Pearsall (1932), Findenegg (1943); Reynolds (1984b, 1998a); Hino et al.(1998), Huszar et al. (2003). Oceans Cyanobacteria Prochlorococcus, Synechococcus, Trichodesmium spp. Bacillariophyceae Rhizosolenia, Bacteristrum, Leptocylindrus Haptophyta Emiliana, Gephyrocapsa, Umbellosphaera Dinophyta Amphisolenia, Dinophysis, Histoneis, Ornithocercus spp. Sources: Riley (1957), Campbell et al.(1994), Karl (1999), Smayda and Reynolds (2001), Karl et al.(2002).

Chronic nutrient deficiencies ratios. The extent to which the N : P gradi- There is, however, another way in which resource- ent underpins, or even correlates with, compo- based competition shapes communities, at least sitional patterns in natural lakes has still to be in oligotrophic waters in which the availability fully resolved. Increasing the phosphorus loads of one or more resources waters is chronically relative to those of nitrogen (thus lowering N : P) deficient and where species having high uptake does result in compositional shifts, often towards affinities for the limiting nutrient(s) are likely dominance by nitogen-fixing Cyanobacteria, as to thrive at the expense of inferior competitors. has been shown in numerous whole-lake fertil- These species are also more likely to provide the isations by Schindler (see, e.g., 1977)andhisco- inocula in future seasons, so the competitive out- workers. The possible responses to simultaneous come is magnified from generation to generation. enrichment with nitrate or ammonium (raising In this way it is relatively easy to hypothesise or maintainingN:P)includefrequentincidences that the selective traits most favoured in chroni- of enhanced production of green algae (especially cally oligotrophic systems – high affinity for lim- Chlorococcales and Volvocales) but they are fre- iting nutrients (Sommer, 1984)andsmall organ- quently confounded by altered carbon dynamics ismic size that is independent of high turbu- and altered trophic effects attributable to the lent diffusivities for their delivery (Wolf-Gladrow activities of grazers (Chapter 6). Seasonal changes and Riebesell, 1997;Section 4.2.1)–selectfor in resourcing (especially with respect to changing the relative absence of large species, for the availabilities with depth) may prompt composi- high incidence of nanoplankters (Gorham et al., tional shifts that may be influenced less by ratios 1974;Watson and Kalff, 1981)and,especially, than by such mechanisms as highly specialised picoplankters, both in lakes (Zuniño and Diaz, affinities, alternative sources of nutrients (nitro- 1996; Agawin et al 2000,Pick2000) and the open genfixation, facultative bacterivory and mixotro- sea (Chisholm et al., 1992;Campbell et al., 1994; phy) or vertical migration. Karl, 1999;Karlet al., 2002;Li,2002). Thus, dis- The idea that species that are simultaneously tinctive groups of species come to characterise limited by different resources do not compete severely P-deficient lakes and ultraoligotrophic but, rather, coexist successfully has a wide fol- oceans (see Table 5.2). lowing among plankton ecologists. It conforms It may well be the case that the lakes can to Hardin’s (1960) principle of competitive exclusion, be described accurately as having high N : P which states a long-standing ecological tenet that 204 GROWTH AND REPLICATION OF PHYTOPLANKTON

true competitors cannot coexist. One of its corol- cessful of the early colonist and pioneer species laries (that, in a steady state, each truly coexist- of the pelagic succession have to be poised to ent species occupies a distinctive niche Petersen invade or to exploit the favourable conditions 1975) has been advanced to account for the mul- that open to them. They may ascend to pre- tiple species composition of natural phytoplank- eminence through an ability to grow faster than ton species assemblages. The resource-based com- their rivals (to ‘outperform’ them but not to ‘out- petition model appears to be powerfully support- compete’ them). Sooner or later, however, grow- ive and, provided the limiting conditions persist ing demands impinge upon the supply of one uninterrupted and for long enough, will lead to or more essential components, after which con- the competitive exclusion of all but the fittest tinued dynamic success requires slightly more species. However, models attempting to verify specialist adaptations for resource gathering. this provision by simulating rather more than Forinstance, noticeably more ‘eutrophic species’ two species competing for more than two limit- might start to exclude oligotrophic ones on ing resources seem to break down into chaos with the basis that the reserve of carbon dioxide is unpredictable outcomes (Huisman and Weissing, depleted as a consequence of plankton growth. 2001). Another possibility is that sufficient growth is accommodated for the light availability in the Discontinuous nutrient deficiences surface mixed layer to become contested by supe- The pattern of change in many pelagic sys- rior light-harvesters. A third likelihood, to which tems is that, as a result of seasonal mixing, particular attention is now given, is that algae storm episodes or periodic inflows, the levels that are able to penetrate deeper in the water of all nutrients may be raised sufficiently to column gain access to nutrients located at depth support the vigorous growth of various species in the increasingly segregated vertical structure. of phytoplankton. The consequence is that the The surface mixed layer is an important available resources are depleted, one or more entity, in limnology as in oceanography. The fre- to a level that represents a threshold of lim- quency with which it is turned over (∼45 min- itation and the ability of some or all species utes or less: see Section 2.6.5)ismuch shorter to grow becomes subject to stress. The initial than the generation time of the plankters embed- combination of relative resource-richness and ded within the layer. It is quite proper, when high insolation supports strong growth of many considering planktic populations, to regard the species in the surface mixed layer. Consequen- surface mixed layer as a single, isotropic envi- tial resource depletion tends to proceed from the ronment. In cold or shallow waters exposed to mixed layer downwards, leading eventually to the moderate wind stress, the surface mixed layer progressive uncoupling of resources from light. extends to the bottom of the water column, or The water column progressively segregates into to within a millimetre or two of the bound- an increasingly resource-depleted upper layer ary layer therefrom. Beyond the density gradi- and to deeper, increasingly light-deficient lay- ent separating mixed layer from deeper, denser ers, wherein available nutrients persist pending water masses, many properties of the habitat exploitation by autotrophs. can differ markedly from those of the surface Such sequences of events are held to differ- mixed layer: renewal rate, temperature, insola- entiate among the adaptive traits and species- tion, gas and nutrient exchange rates, and so on. specific performances of phytoplankton, deeply Thus, the variability in its vertical extent can also influencing the species selection and seasonal be a critical determinant of performance, alter- shifts in species dominance. These progressions nately entraining and randomising the planktic of composition and dominance are sufficiently population through a column of uniform and striking, in some cases, to have been analo- increasingly low insolation, then disentraining gised to classical ecological successions in terres- it through stagnating layers. The frequency of trial plant communities (Tansley, 1939;Reynolds, thealternation can be critical too: segregation 1976a;Holliganand Harbour, 1977). The most suc- may last for a few hours (as in dielly stratifying REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 205 systems), a few days (polymictic and atelomictic form resistance are essential to embedding, so systems), months on end (seasonal stratification) large size and low form resistance are advan- or more or less continuously (as in meromic- tageous to ready disentrainment from weaken- tic systems). The longer is the separation, the ing turbulence and to commencing controlled, greater can be the differentiation with, instead directed excursions through the water column. of one, unique environment, a continuous and The velocities achieved can nevertheless seem widening spectrum of individualistic microhab- impressive. Smaller gas-vacuolate, bloom-forming itats (Reynolds, 1992c;Floder,¨ 1999). Simultane- Cyanobacteria (including Microcystis, Gompho- ous feedbacks, including the transfer of settling sphaeria, Gloeotrichia, Nodularia, Cylindrospermopsis, biomass, cadavers and the faecal pellets of algal raft-forming Aphanizomenon and the species of consumers to the uninsolated layersbelow,may Anabaena and Anabaenopsis which typically aggre- further enhance the developing structural dis- gate into secondary tangles of filaments) whose continuity. buoyant velocites may reach 40–100 µms−1 Among the species attempting still to assem- normally sink three to six times more slowly ble biomass and replicate their numbers, there (say 0.6–3.0 m d−1)(Reynolds, 1987a). The move- is a progressive transfer of advantage from those ments of large freshwater dinoflagellates like Cer- adept at exploiting the mixed-layer resource base atium hirundinella and Peridinium gatunense can (high-sv−1 species, sustaining high replication cover 8–10 m in a single night (Talling, 1971; rates) to those which are equipped to benefit Pollingher, 1988). The rates quoted for many from the separation of the resource base. The marine species exceed 100 µms−1;oneortwo situation is reminiscent of the progressive ele- exceed 500 µms−1 (Smayda, 2002), although vation of productive terrestrial foliage from the the distances they travel are not given. Volvox herb layer to the woodland canopy. In the case undertakes the longest reported circadian migra- of the pelagic, however, it is the downreach of tion of any freshwater flagellate, traversing 17 m the resource-gathering capacity that is respon- in either direction of the Cabora Bassa Dam, sible for the functional separation rather than Mozambique (Sommer and Gliwicz, 1986), at an theuplift of the light-harvesting apparatus! The average velocity scarcely under 1.5 m h−1.Inabso- investment by (appropriately adapted) terrestrial lute terms, this is modest but, at the scale of the plants is in building the mechanical connection. organism, progression at the rate of 1 to 3 colony- Among the microscopic pelagic plants the adap- diameters per second is impressive. tive investment is in migration. The question has to be asked whether these Twointerrelated sets of adaptations give the migrations do actually yield a harvest of nutri- advantage to pelagic canopy species. One is the ents, sufficient to provide a dynamic advan- power of motility: if the alga is to have any tage over non-migrating species. According to prospect of covering the vertical distance sep- Pollingher (1988), patterns of movement are arating light and nutrient resources, it must dominated by a strong, positive phototaxis in be able to determine the direction of its move- the early part of the day (though, generally, ment. Flagellate genera of the Cryptophyta, their movements will avoid supersaturating light the Pyrrhophyta, the Chrysophyta, the Eugleno- intensities) but they show a decining photo- phyta and the Chlorophyta would appear to responsiveness during the course of the solar have the essential preadaptations, although the day. The quality of the light and temperature buoyancy-regulating mechanism of gas-vacuolate gradients, the extent of nutrient limitation and Cyanobacteria is just as effective a means of pro- theage of the population also influence pat- pelling migratory movements. The second adap- ternsofmovement. The extent of dinoflagellate tation, however, is the one that turns the ability migrations in a given lake are said to increase to move into the ability to perform substantial with decreasing epilimnetic nutrients, provided vertical migration, i.e. the size-determined capac- thesegregated structure persists and the excur- ity to disentrain from residual turbulence (Sec- sions into deeper water provide reward. It is inter- tions 2.7.1, 2.7.2). Just as small size and maximun esting, too, how diminishing nutrient resources 206 GROWTH AND REPLICATION OF PHYTOPLANKTON

should determine that less of the photosynthate direction enables an alga to recover vertical sta- produced by buoyancy-regulating Cyanobacteria tion very quickly in the wake of disruptive mix- ends in new cytoplasm and more goes to offset- ing events, when smaller flagellates or solitary ting buoyancy, forcing organisms to sink lower buoyany regulating filaments take hours or days in the water column (Sas, 1989). Note that short- to do so (Reynolds, 1984c, 1989b). Another is that age of carbon, like shortage of light, means less in the face of weak wind- or convective-mixing, photosynthate is produced, so organisms become the alga can be quite effective in self-regulating lighter and float closer to the surface. This prin- its vertical position in order to balance its pho- ciple has been demonstrated well in the obser- tosynthetic production and its resource uptake vations and experiments of Klemer (1976, 1978; with the rate of cell growth and replication. In Klemer et al., 1982, 1985)andSpencer and King this way the cell saves energy in fixing photo- (1985). These self-regulated movements of large synthate, which, if it could not be made into plankters certainly seem to open the access to proteins and new cell material, would otherwise deep-seated nutrient stores. It is apparent, too, have to be voided from the cell. Organisms which that their growth may be enhanced when con- do this very well, such as Microcystis,not only rise ditions of near-surface nutrient depletion obtain to dominance but remain dominant for months and the range of vertical migration extends to (and even years on end) when the appropriate depths offering replenishment. conditions persist (Zohary and Robarts, 1989). There are few studies that provide compelling evidence that this is always the case Low insolation and growth-rate regulation (Bormans et al., 1999). However, Ganf and Oliver Under conditions of short photoperiods and low (1982)showed, through observation and careful aggregate insolation, the problem for phyto- experimental translocation, that Anabaena fila- plankton is defined by the point that the alga ments picked up substantial amounts of nutri- is no longer able to intercept and harvest suffi- ent on their buoyancy-regulated excursions in cient light energy, or to invest it the recruitment the Mount Bold Reservoir, South Australia. Raven of new protoplasm and daughter biomass, at a and Richardson (1984) considered the extra nutri- rate that the temperature and the nutrient sup- ents derived by a migrating marine Ceratium to ply will allow. Below this level, growth rate is, be only weakly attributable to movement per se indeed, light-limited. The curves inserted in Fig. (see Section 4.2.1)and much more to the encoun- 5.4 differentiate among plankters on the basis of ters with unexploited nutrients in the (to them) their shape and their capacity for low-light adap- accessible parts of the water column. Deep-water tation. The point to notice is that the species reserves of phosphorus were shown to be within that are capable of the fastest rates of growth thefacultative swimming ranges of Ceratium in under relatively high insolation are not necessar- Esthwaite Water, UK (Talling, 1971)andwithin ily the best adapted to live on small light doses. the‘vertical activity ranges’ of Ceratium (and, for The limnetic species that do this well include atime, Microcystis)intercepted by sediment traps the diatom Asterionella and solitary filamentous in Crose Mere, UK (Reynolds, 1976b). species of the Oscillatoriales (Planktothrix agardhii, Thus, strong, self-regulated motility is con- Limnothrix redekei), in which the capability is cor- sidered to offer significant advantages, provid- related with relative morpholgical attenuation ing opportunities for the selective garnering of (high msv−1:Fig.5.5). There is often a high capac- thediminishing resources of a structured envi- ity for auxillary and accessory pigmentation as ronment. Adapted species are enabled access to well. Thus, their successful contention to per- parts of the water column that other algae do form relatively well in poorly insolated, natural not reach, or do not do so sufficiently quickly, mixed layers owes most to their extraordinary or, having done so, cannot reverse their motion to abilities to open the angle of r on I (Fig. 5.4; αr recover a position in the euphotic zone. It should in Fig. 5.5)and,thus,tolowerthe light inten- not be assumed that this is the only advantage. sity at which growth rate can be saturated. In The ability to swim strongly and in controlled theopen, mixed-water column, this extends the REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 207 actual depth through which growth-saturating tons m−2 s−1), the light-limited Asterionella might photosynthesis may be maintained and, in turn, still increase at a rate of 0.335 d−1, which is lengthens the aggregate of probabilistic photope- twice as fast as that of the temperature-limited riod, tp,overthat expected for unadapted species Planktothrix or the light-limited Chlorella.Itis in the same water layer. From the least-squares at once appreciable how subtle are the condi- regression fitted to the data in Fig. 5.5, tions distinguishing among species performances − . under low doses of light. We might also spec- α = 0.257(msv 1)0 236 (5.8) r ulate that although there is an apparent dis- it may be predicted that the stellate colony of cretion in favour of diatoms in cold, energy- Asterionella generates a slope of αr = 0.86 (mol deficient, mixed layers, a little more vigourous − photon) 1 m2, while for a 1-mm thread of Plankto- mixing (I∗ falls) or a lessseverewintertem- thrix agardhii, αr = 1.12. For the small spherical perature might favour filamentous Cyanobac- cell of Chlorella,theslope is predicted to be only teria instead. Reduced mixing and better near- − 0.39 (mol photon) 1 m2.Analogous to the inter- surface insolation immediately favours faster relationships among photosynthetic rate and the growing nanoplankters such as Chlorella. onset of light saturation of photosynthesis (Eq. 3.5,Section 3.3.1), the lowest light dose that will sustain maximal growth rate at 20 ◦Cisindicated Trait interaction and functional /α by thequotient, r20 r. Thus, on the basis of the differentiation in phytoplankton assembled data (see Table 5.1), we may deduce The real world of phytoplankton is a blend that Chlorella growth will be saturated by a pho- of deficiencies of differing intensity and fre- ton flux of 3.34 mol photons m−2 d−1 (equivalent quency, especially with respect to the availabil- toaconstant∼39 µmol photons m−2 s−1), that of ity and accessibility of nutrient resources and Asterionella by 2.07 mol photons m−2 d−1 (24 µmol thesolar energy needed to process them. Spe- photons m−2 s−1), and that of the Planktothrix by cialist adaptatations, both in terms of physio- 0.77 mol photons m−2 d−1 (9 µmol photons m−2 logical responses at the scale of the life cycle s−1). and the traits distinguished at the evolution- The inference is emphasised: at irradiance lev- ary scales, may increase the relative fitness of els exceeding levels of 3.34 mol photons m−2 some species along particular gradients of envir- d−1, Chlorella is the ‘fittest’ of the three, and its onmental variability but none is well suited to regression-predicted growth rate of 1.84 d−1 out- all conditions. For instance, we may suppose that strips those of Asterionella (1.78 d−1)andPlank- themost competitive adaptation would be to tothrix (0.86 d−1). However, at light levels equiv- enable the phytoplankter to self-replicate more alent to 0.77 mol photons m−2 d−1, Planktothrix rapidly than other species that might be present; can still be argued to be able to maintain its max- hence, a morphology conducive to rapid surface imum growth rate (0.86 d−1), and when that of exchanges of nutrients should be favoured, that Asterionella is cut back to 0.66 d−1 and Chlorella is is, one that maintains a large sv−1. The oppos- severely light-limited at not more than 0.42 d−1. ite trend of increasing size (and reducing sv−1) When the low temperatures of high-latitude win- carries advantages of motility, storage and per- ters are taken into account, the impact of surface- sistence (see also Section 6.7), where the ability to-volume relationships modify the relative fit- to influence vertical position, to gain access to nesses of these organisms. At 5 ◦C, the predicted nutrient resources unavailable to other species resource-saturated growth rates for Chlorella, and to avoid consumption by herbivores offer Asterionella and Planktothrix are, respectively, superior prospects of survival. One advantage has 0.375, 0.335 and 0.163 d−1 and the respective sat- been ‘traded’ against another, at the price of low- urating fluxes are calculated to be 0.96, 0.39 and ered habitat flexibility: some environments will 0.15 mol photons m−2 d−1. Thus, under an aver- be better tolerated, or even preferred, by a given age irradiance (I∗)of0.4 mol photons m−2 d−1 species than will others. Such differentiation is, photon flux (equivalent to a constant 5 µmol pho- of course, the basis of patterns in the spatial 208 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.8 Comparison of growth-rate performances of some phytoplankters. In (a), the minimum light intensity (I) and the minimum soluble-phosphorus concentration ([Slim]) required to saturate the growth at 20 ◦Cofthe named algae are plotted against each other. The algae are: Ast, Asterionella; Chlo, Chlorella; Mic, Microcystis; Per, Peridimium cinctum; Pla, Planktothrix agardhii.Inthe other sub-ﬁgures, selected isopleths of growth rate at 20 ◦C (inserted numerals are × 10−6 s−1)are constructed against the same gradients, for (b) Chlorella, (c) Asterionella and (d) Microcystis. The contours are Redrawn with permission from Reynolds (1997a).

and temporal distribution of species, whereby against axes representing steady-state concentra- some are more clearly associated with particular tions of phosphorus and the photon flux of white conditions than are others. The further adaptive light, at 20 ◦C. The high levels of resource and option for larger algae – that of shape distortion light required to saturate the most rapid growth that increases the surface area bounding a given of Chlorella show well against the requirements of cytovolume – provides not so much a compromise four others species (Fig. 5.8a). The sensitivity of between small and large size but the enhanced Chlorella performance to both light and phospho- ability to process resources into biomass in rela- rus relativetothat of Asterionella or of the poorly tively short periods of exposure to light. performing Microcystis against these two criteria Based upon the growth rates of various is evident (Fig. 5.8b, c, d). species of algae against chosen dimensions in the foregoing sections, we are now able to devise comparative graphical representations of Growth and reproductive strategies thereplicative performances of algae against the When growth under persistently low levels of two key axes of resource availability and inso- light and nutrient are considered simultane- lation. In Fig. 5.8a, growth-rate contours of sev- ously, the basis for some of the very interesting eral algae are drawn in space defined by light patterns alluded to by Tilman et al.(1982)and and phosphorus saturation of growth-rate poten- by Sterner et al.(1997)may be readily appreci- tial. The result is broadly similar to those built ated. Now, for example, we may envisage circum- on mean underwater light levels and KU val- stances under which growth rate in Asterionella ues with respect to species-specific phosphorus is encountering (say) silicon limitation when the uptake rates (Reynolds, 1987c)oroflightsup- growth rate of Cyclotella is constrained by light, ply and nutrient supply (Huisman and Weiss- and when the growth rate of Planktothrix is too ing, 1995). The plots making up the rest of Fig. constrained by low temperature or low phosphor- 5.8 show species-specific replication-rate contours us to be able to take full advantage. REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 209

There are probably sufficient data to be able ing resources in short supply with their reten- to simulate these interactions more rigorously. tion among a high survivorship. Unlike the obli- This is less interesting to pursue than it is to gately fast-growing, r-selected category, resource- abstract the generalities about the differing adap- (K-)selected species do not share the constraint of tations shown by the algae considered here and maintaining a high surface-to-volume (sv−1)ratio. the broad properties that underpin their strate- However, the acquisitive garnering of dimin- gies for growth and survival. The use of the word ishing resources sometimes favours significant ‘strategy’ in the context of the evolution of life powers of migratory motility, for which a rel- histories is open to criticism on etymological atively large size (with attendant penalties in grounds, as it implies that their differention is reduced sv−1,slowgrowthrateandimpaired planned or anticipated in advance (Chapleau et light-absorption efficiency, εa)isessential (see al., 1988). In reality, different patterns for pre- Sections 2.7.1, 3.3.3). Microcystis aeruginosa pro- serving and reproducing genomes have evolved vides a good example of this second type of along with the organisms they regulate and, just strategy that identifies ‘winners’, or like Aesop’s as certainly, have been shaped by the same forces fabled tortoise, the ‘good competitor’ in the sense of natural selection. The patterns are distinctive, understood by most plankton ecologists (Kilham separating life histories that, for example, permit and Kilham, 1980). opportunistic exploitation of resources and pho- The ability to harvest and process energy from ton energy (as does Chlorella in the example in low or diminishing irradiances or from truncated the previous section)or,alternatively, may pro- opportunities at higher irradiance is favoured by vide high adaptability to a low nutrient or to low small size or by attenuation of larger sizes (in energy supply (as does Planktothrix). The compar- one or possibly two) planes. These traits repre- ative efficiencies and flexibilities of investment sent a high photon affinity, which is not bound of harvested energy and gathered resources into exclusively to either r- or K-selection, and to species-specific biomass define the growth and which Reynolds et al.(1983b) applied the term reproductive strategies of phytoplankton (Sandgren, w-selection. 1988a). There are clear similarities and apparent So far, the discussion has identified three analogies in these broad distinctions with the basic sets of strategic adaptations, involv- three primary ecological and evolutionary strate- ing morphologies, growth rates and associ- gies identified among terrestrial plants (Grime, ated behaviours. The first is the Chlorella type 1977, 1979, 2001). Grime’s concept was built of exploitative or invasive strategy, in which around the tenability of habitats according to (i) organisms encountering favourable resource the resources available and the levels of stress on and energy fluxes can embark upon the life cycles that resource shortages might impose rapid resource processing, biosynthesis and on plant survival and (ii) the duration of these genomic replication (reproduction) that consti- conditions, pending their disruption or obliter- tute growth. They necessarily have a high growth ation by habitat disturbance. Of the four possi- rate, r,based on an ability to collect and con- ble permutations of stress and disturbance (Table vert resources before other species do and, in this 5.3), one, the combination of continuous severe sense (the one followed by most plant ecologists), stress and high disturbance results in environ- they are ‘good competitors’. Curiously, plankton ments hostile to the establishment of plant com- ecologists reserve this term for the ‘winners’ of munities is untenable. These are deserts! The the competition, applying it to those species that three tenable contingencies are variously pop- specialise in the efficient garnering, conserving ulated by plants specialised in either (a) rapid and assembling the limiting resource base (K) exploitation of the resources available (‘com- into as much biomass as it will yield. Thus, petitors’ in the original usage of Grime 1977, thesecond set of strategic adaptations variously 1979), which he dubbed ‘C-strategists’; or (b) tol- combines high resource affinity and/or special- erance of resource stress, by efficient matching ist mechanisms for obtaining scarce or limit- of the limited supply to managed demand, and 210 GROWTH AND REPLICATION OF PHYTOPLANKTON

Ta b l e 5.3 Basis for evolution of three primary strategies in the evolution of plants, C R Monor phytoplankton and many other groups of organisms Syn Chlo Plg Fra Habitat productivity Scq Ast 0 Monod Habitat 10 Chla Din Lim r duration High Low Sth Tab Aul

− 1 Pla ag Long Competitors, Stress-tolerant Aph

µ m Cry invasive (C ) (S ) / Short Disturbance- No viable strategy − 1 Ana Cer sv Per tolerant 10−1 ruderals (R) Eud S Source:Original scheme of Grime (1979; modiﬁed Mic after Reynolds, 1988a;Grime, 2001). Vo l 10−2

101 102 103 msv−1

Figure 5.10 Morphological ordination of some species of freshwater phytoplanton, against axes invoking maximal linear dimension (m), surface area (s) and volume (v)ofthe vegetative units, with the C-, S- and R-strategic tendencies. The algae are: Ana, Anabaena flos-aquae; Aphan, Aphanizomenon flos-aquae; Ast, Asterionella formosa; Aul, Aulacoseira subarctica; Cer, Ceratium hirundinella; Chla, Chlamydomonas; Chlo, Chlorella sp.; Cry, Cryptomonas ovata; Din, Dinobryon divergens; Eud, Eudorina unicocca; Fra, Fragilaria crotonensis; Lim r, Limnothrix redekei; Mic, Microcystis aeruginosa; Monod, Monodus sp.; Monor, Monoraphidium contortum; Per, Peridinium cinctum; Pla ag, Planktothrix agardhii; Plg, Plagioselmis nannoplanctica; Scq, Scenedesmus quadricauda; Sth, Figure 5.9 Grime’s model of tenable and untenable Stephanodiscus hantzschii; Syn, Synechococcus sp.; Tab, Tabellaria habitats, and noting the primary (C, S or R) life-history flocculosa var. asterionelloides; Vol, Volvox aureus. Redrawn with strategies required to secure survival. Redrawn, with permission from Reynolds (1997a). permission from Grime (2001).

to which he gave the label ‘S-strategists’; or (c) respectively, C, S or R strategies, on the satisfying tolerance of disturbance, through making good basis of agreement among the morphological opportunity of transient habitats and interrupted properties, growth rates and life-history traits. opportunities to process resources into biomass The distribution of phytoplankton species (‘R-strategists’). according to their individual morphologies The three primary strategies of Grime’s CSR plotted against axes of sv−1 and msv−1 (Fig. 5.10). model form the apices of a triangular ordination Just as with Grime’s (1979)scheme, species are (Fig. 5.9), which representation readily allows not exclusively C or S or R in their strategic the accommodation of numerous intermediates adaptations. Many species of phytoplankton and trait-combinations. Reynolds (1988a, 1995a) show intermediate characters. Interestingly, found only minor difficulties in analogising intermediacy in morphological and physiolog- the r-, K- and w-selected groups to exemplifying, ical characters matches well the intermediacy REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 211 of their ecologies. The C–S gap is spanned by tion recognises that motility and large size genera such as Dinobryon, Dictyosphaerium, are not necessary adaptations to function in Coenochloris, Pseudosphaerocystis, Eudorina and, chronically very resource-depleted pelagic envi- arguably, Volvox (Reynolds, 1983b), and by ronments. Indeed, resource gathering in spatially Aphanocapsa and Aphanothece. The series spans continuous, rarefied environments is favoured diminishing sv−1 ratios, maximum growth rates by small size, whereas the low levels of dif- and low-temperature tolerance but increas- fuse biomass is an unattractive resource for ing ability to exploit and conserve nutrient direct grazing by mesozooplankters (see Chap- resources. Algae in the C–R axis include predom- ter 6). The adaptive strategies for surviving inantly centric diatoms of varying tolerance of the‘resource desert’ of the ultraoligotrophy of turbidity and the Scenedesmus–Pediastrum element the oceanic pelagic are accorded the additional of enriched shallow ponds and rivers). The R–S stress-tolerant category SS. possibility is represented by the slow-growing, The original ascriptions of C, S and R cate- long-surviving, acquisitive but highly acclimated gories to phytoplankton (Reynolds, 1988a)sepa- species of density gradients, like Planktothrix rate quite satisfactorily on the plot of the areas rubescens and Lyngbya limnetica.Certain (not projected by various species of phytoplankton all) members of the genus Cryptomonas show a and the product of maximum dimension and blend of the characteristics of all three primary surface-to-volume ratio (msv−1)Fig.3.12). Near- strategies in being unicellular, having cells of spherical forms align close to msv−1 [d × 4π(d/2)2 moderate size (1–4 ×103 µm3)andofinterme- ÷ 4π(d/2)3/3] = 6but separate broadly in to diate sv−1 (0.3–0.5 µm−1), and being capable of C and S species according to size, because the −6 intermediate replication rates (r20∼10 × 10 carbon and chlorophyll contents vary with v = −1 −6 −1 3 s ; r0∼0.9 × 10 s ). 4π(d/2) /3but the light interception increases It is right to point out that Grime’s CSR con- as a function of the disk area, a = π(d/2)2. cept of plant stategies is not universally accepted The morphological attenuation of the R species and it has been subject of vehement and chal- pulls out the plot to much higher msv−1 val- lenging debate (see Tilman, 1977, 1987, 1988; ues. Thus, we distinguish species that are capa- Loehle, 1988, a.o.). Although there is much com- ble of rapid growth in benign, resource-replete mon ground shared by the adversaries and, in environments, those that are able to go on truth, the differences are more of perspective squeezing out increased biomass from diminish- and emphasis (Grace, 1991), the differences have ing light income and those who are physiolog- never been entirely resolved. The application to ically or behaviourally adapted to function in plankton has not been so criticised and some spite of developing nutrient stress. The model (Huszar and Caraco, 1998;Fabbroand Duiven- appears in various guises later in the book, vorden, 2000;Gosselain and Descy, 2000;Kruk demonstrating the power and flexibility of the et al., 2002;Padisak,´ 2003)butbynomeans strategy–process–ecosystem interactions. It even all (Morabito et al., 2002), have found the argu- provides the bridge to the light : nutrient hypoth- ments convincing and helpful to interpretation. esis (Sterner et al., 1997)insofarasthespecies The applicability of a scheme devised for plant best adapted to cope with low doses of I∗ are most species is not a barrier: it is now quite evi- able to cope with high particulate content in the dent that the idea has a long pedigree among waterandtheC:Pratioofthesestonavailable other ecological schools (Ramenskii, 1938)and to secondary consumers. has been applied successfully to the ‘violent’, ‘patient’ and ‘explerent’ strategies of zooplank- 5.4.6 Resource exhaustion and survival ton (Romanovsky, 1985). The CSR model has been It is reasonable to assume that the growth of applied to fungi (Pugh, 1980)andperiphyton phytoplankters distinguished by efficient, high- (Biggs et al., 1998). affinity resource-gathering capabilities may con- An updated application to phytoplankton tinue until they deplete their growth-limiting is set out in Box 5.1.Anotable modifica- resource to near exhaustion. It was often and 212 GROWTH AND REPLICATION OF PHYTOPLANKTON

Box 5.1 Summary of behavioural, morphometric and physiological characteristics of growth and survival strategies of freshwater phytoplankton

With little adjustment, the primary strategies (otherwise, functional types) of plants devised by Grime (1979, 2001) are known to apply to other types of organism, including phytoplankton. The application of the scheme to plankton (Reynolds, 1988a) required some modest adjustment but the relevant morphological and physiological characteristics are, of course, peculiar to planktic algae. These are listed below, following Reynolds (1988a, 1995a)but include the features of a new subcategory (SS)toaccommodate features of permanent stress-tolerant algae of ultraoligotrophic oceans. C strategists Grime’s name Competitors Reynolds’ (1995a) label Invasive opportunists Dispersal Highly effective, cosmopolitan; mechanisms sometimes obscure Selection r Cell habit Mostly unicellular Unit sizes 10−1–103 µm3 msv−1 6–30 Cell projection >10 m2 (mol cell C)−1 > × −6 −1 > −1 r 20 10 10 s ; 0.9 d > × −6 −1 > −1 r 0 2 10 s ; 0.18 d Q10 <2.2

Species experience low growth thresholds for light (Section 5.5), have generally low rates of sinking (some are motile; Section 6.3) and are highly susceptible to grazing zooplankton (Section 6.4). Representative genera Chlorella, Ankyra, Chlamydomonas, Coenocystis, Rhodomonas. R strategists Grime’s name Ruderals Reynolds’ (1995a) label Attuning or acclimating (also processing– constrained) Dispersal Widely distributed, mechanisms sometimes obscure Selection r and K (w in Reynolds et al., 1983b) Cell habit Some unicellular, many coenobial Unit sizes 103–105 µm3 msv−1 15–1000 Cell projection 8–30 m2 (mol cell C)−1 > × −6 −1 > −1 r 20 10 10 s ; 0.85 d × −6 −1 > −1 r 0 0.08–2 10 s ; 0.1 d Q10 2.0–3.5

Species force very low growth thresholds for light (Section 5.6), sinking rates low to high, most are non-motile (Section 6.2); some susceptible to grazing zooplankton REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 213

(Section 6.3). Representative genera Asterionella, Aulacoseira, Limnothrix, Plank- tothrix. S strategists Grime’s name Stress-tolerators Reynolds’ (1995a) name Acquisitive (also resource-constrained). Dispersal Tendency to discontinuous distribution, mechanisms better known Selection Strongly K Cell habit Some unicellular, many coenobial Unit sizes 104–107 µm3 msv−1 6–30 Cell projection <2.5 m2 (mol cell C)−1 < × −6 −1 < −1 r 20 8 10 s ; 0.7 d < × −6 −1 < −1 r 0 1 10 s ; 0.09 d Q10 >2.8

Species contend effectively with diminishing, or increasingly distant nutrient resources, either through exploiting alternative sources (nitrogen ﬁxation, phosphatase production, phagotrophy on bacteria or particulate organic material). Most are motile, some are strongly so, sinking rates low but may undertake controlled migrations over large vertical distances. Also referred to as resource ‘gleaners’ (Anderies and Beisner, 2000). Representative genera Microcystis, Anabaena, Gloeotrichia, Ceratium, Peridinium, Chrysosphaerella, Uroglena. SS strategists Grime’s name (not applicable) Reynolds’ (1995a) Chronic-stress tolerant name Dispersal Cosmopolitan Selection Ultimately K Cell habit Exclusively unicellular Unit sizes ≤4 µm3 msv−1 6–8 Cell projection ∼50–60 m2 (mol cell C)−1 > × −6 −1 > r 20 unknown, probably 20 10 s ; 1.8 d−1 × −6 −1 −1 r 0 Possibly up to 0.5 10 s ,0.4d Q10 Not known, probably ∼2

This newly separated group of species tolerant of chronic nutrient stress accommodates the prokaryotic picoplankters that dominate the rarefied environments of the tropical seas and which, increasingly, have been shown to be active in the open waters of the world’s largest and most oligotrophic lakes (Reynolds et al., 2001). They are non-motile but have very low sinking rates. Their small size is the keytoliving on very dilute nutrient sources. It would leave them very vulnerable to grazing by filter-feeders, except that they inhabit environments that fail to sustain filter-feeding zooplankton. Representative genera Prochlorococcus (in the sea; Cyanobium, Cyanodictyon are considered to be limnetic analogues). 214 GROWTH AND REPLICATION OF PHYTOPLANKTON

commonly supposed by many plankton ecolo- of reproductive and resting propagules has been gists that nutrient exhaustion is followed by mass mainly confined to studies on particular phyloge- clonal mortalities. This view was perhaps encour- netic groups (Sandgren, 1988a). It is not inappro- aged by numerous observations of ‘bloom col- priate to give a brief perspective at this point. lapse’, of diatoms running out of silicon (e.g. Resting stages come in a variety of forms and Moed, 1973)orthephotolysis of surface scums of are stimulated by a variety of proximate events Cyanobacteria (e.g. Abeliovich and Shilo, 1972). and circumstances, and their success in ‘carrying These relatively impressive eventualities apart, forward’ biomass and genomes is also quite vari- however, phytoplankters are rather better pre- able. Among the simplest resting stages are the pared than this to be able to avoid sudden death contracted protoplasts produced in such centric and disintegration. Depletion of one of the essen- diatoms as Aulacoseira (Lund, 1954) and Stephano- tial resources usually leads to a cellular reserve of discus spp. (Reynolds, 1973a). These form quite the others and thecellmaybeable to use stored freely in cells falling into aphotic layers and may carbohydrate, polyphosphate or protein reserves be prompted by microaerophily and low redox, to maintain some essential activity. However, it which conditions may be tolerated for a year is quite clear that it is better for the cell to lower or more. The contents pull away from the wall, its metabolism and to close down those processes abandon the central vacuole and shrink to a tight not directly associated with actually staying alive. ball, a micrometre or so in diameter. Individual Earlier chapters have emphasised the mecha- cells or filaments containing resting stages lit- nisms for internal communication of nutrient- terthe surface sediments. If seeded sediment is uptake activity of the membrane- transport sys- placed under low light in the laboratory, Aulaco- tem (Section 4.2.2), the activation of inhibitory seira will ‘germinate’ and produce swathes of new nucleotides (such as ppGpp) in response to falling filaments in situ.Germination in nature may be amino-acid synthesis (Section 4.3.3)andthesus- only a little less spectacular but it always depends pension of nuclear division (Section 5.2.1). Each upon the resuspension of filaments and cells by represents a step in the biochemical procedure by entrainment from sediments accessible to tur- which the cell senses its environmental circum- bulent shear. Thus, formation and germination stances and organises its appropriate defences to of the resting stages is governed by the activity enhance its survival prospects. These may include or otherwise of its photosynthetic capacity. Per- the inception of a ‘cytological siege economy’ haps 5–20% of the sedimenting population may and the structural reorganisation of the proto- form resting stages. The percentage of these that plast into resting cells, with or without thickened return to the plankton is probably small but they walls. can provide quantitatively important inocula to The biological forms of most kinds of rest- future populations (Reynolds, 1988a, 1996b). ing cell are well recognised by plankton ecolo- The Cyanobacterium Microcystis has the abil- gists and, in many cases, so are the environmen- ity to control its own vertical migrations through tal attributes which induce them. Equally, the regulating its buoyancy and, in warm latitudes, implicit benefit of survival of resting stages is it may move frequently (perhaps dielly) between widely accepted as a means to recruit later pop- sediment and water, very much as part of ulations from an accumulated ‘seed bank’. They its vegetative activity (May, 1972;Ganf, 1974a; need to recognise and respond to their reintro- Tow, 1979). In temperate lakes, Microcystis is fre- duction into favourable environments or to ame- quently observed to overwinter on the bottom liorating conditions by embarking upon a phase sediments (Wesenberg-Lund, 1904; Gorham, 1958; of renewed vegetative growth. However, it has to Chernousova et al., 1968;Reynolds and Rogers, be stated that, in marked contrast to the efforts 1976;Fallonand Brock, 1981; and many others that have been made to observe and under- reviewed in Reynolds, 1987a). There is a mas- stand the mechanisms generating the spatial sive autumnal recruitment of vegetative colonies and temporal patterns of phytoplankton occur- from the plankton to depth (Preston et al., 1980), rence, detailed information on the significance where they enter a physiological resting stage. REPLICATION RATES UNDER SUB-IDEAL CONDITIONS 215

No physical change occurs (they do not encyst) colonies apparently need the low temperatures and chlorophyll, as well as a latent capacity and low oxygen levels for their maturation. Ulti- for normal, oxygenic photosynthesis, is retained mately, they also require low oxygen levels and (Fallon and Brock, 1981). Curiously, the cells simultaneous low insolation to persuade them also remain gas-vacuolate. Despite being (ini- to initiate the formation of the new colonies tially) loaded with glycogen, other carbohydrates, that recolonise the water column in the follow- proteinaceous structured granules and polyphos- ing year (Reynolds and Bellinger, 1992;Brunberg phate (Reynolds et al., 1981), they would be buoy- and Blomqvist, 2003). The completion of this ant but for the precipitation of iron hydroxide cyclical process depends on interactions among on the colony surfaces, which acts as ballast light, temperature and sediment oxygen demand. and causes the organisms to sink (Oliver et al., Whereas upwards of 50% of the colonies consti- 1985). Once on the sediments, in very weak light tuting the previous summer maximum number and at low temperatures, they experience con- of colonies may settle to the sediments, ≤10% siderable mortalities, although some cells live might contribute to the re-establishment of a on under these conditions, apparently for several summer population the following year (Preston years insomecases (see Livingstone and Cambray, et al., 1980;Brunberg and Blomqvist, 2003; 1978). The surviving cells function at a very low Ishikawa et al., 2003). metabolism and are tolerant of sediment anoxia It may be noted that Microcystis colonies also (and consequent re-solution of the attached iron) survive in microenvironments created by down- but there are, by now, too few of them to lift the wind accumulations of surface scums on large erstwhile colonial matrix back into the water col- lakes and reservoirs, especially where warm sum- umn. mers, high energy inputs and high upstream Reinvasion of the water column follows a nutrient loadings are simultaneously prevalent. phase of in-situ cell division, in which clusters of Good examples come from the reservoirs of the young cells are formed, constituting a pustule- Dnieper cascade (Sirenko, 1972)andtheHart- like structure that buds out of the original, beespoort Dam in South Africa (Zohary and ‘maternal’ mucilage matrix, until it is released Robarts, 1989). The conditions in these thick, or it escapes into the water. The process was copious ‘crusts’ or ‘hyperscums’ are effectively described originally by Wesenberg-Lund (1904), lightless and strongly reducing (Zohary and Pais- but the information was largely ignored. The Madeira, 1990)but, save those actually baked dry ‘nanocytes’ found by Canabeus (1929)and,later, at the surface, Microcystis cells long remain viable ‘rediscovered’ by Pretorius et al.(1977), seem to and capable of recovering their growth. refer to the young, budding colonies. Sirenko Many species respond to the fabled ‘onset (pesonal communication quoted in Reynolds, of adverse conditions’ by producing morphologi- 1987a) has viewed the entire sequence, claim- cally distinct resting propagules. Among the best ing that the potential mother cells are identi- known are the cysts of dinoflagellates, which fiable in advance by their larger size and more are sufficiently robust to persist as a fossils of intense chlorophyll fluorescence. The process has palaeontological significance (for a review, see also been reproduced under controlled condi- Dale, 2001). Some 10% of the 2000 or so marine tions in the laboratory (Caceres´ and Reynolds, species are known to produce resting cysts. In 1984), using material sampled from autumnal some instances, they are known, or are believed, sediment. It requires the exceedence of a tem- to be sexually produced hypnozygotes. The cell perature and insolation threshold and it occurs walls in many species contain a heavy and com- more rapidly while anaerobic conditions perplex organic substance called dinosporin, chem- sist. These conditions have to be mirrored in ically similar to sporopollenin of higher-plant natural lakes of the temperate regions before pollen grains. Some species deposit calcite. In Microcystis colonies begin to be recruited to the thelaboratory, cyst formation may, indeed, be water column in the spring. Sediments have to induced by nutrient deprivation and adverse retain colonies through the winter period, where conditions but the regular, annual formation 216 GROWTH AND REPLICATION OF PHYTOPLANKTON

of cysts in nature (coastal waters, eutrophic tal adequacy but which are tenanted briefly by lakes) possibly occurs in response to cues that vegetative populations. anticipate ‘adverse’ conditions rather than the In contrast, nostocalean Cyanobacteria pro- actual onset of those adversities. The protoplasts duce their asexual akinetes in rapid response of newly formed cysts usually contain conspicu- to theonset of physiological stress. Akinetes are ous reserves of lipid and carbohydrate, accumu- the well-known ‘resting stages’ of such genera as lated during stationary growth (Chapman et al., Anabaena, Aphanizomenon and Gloeotrichia (Roelofs 1980). The number of cysts produced by fresh- and Oglesby, 1970;Wildman et al., 1975;Rother water Ceratium hirundinella in autumn has been and Fay, 1977;Cmiech et al., 1984). These, too, estimated from the sedimentary flux to account have typically thickened external walls, within for ≤35% of the maximum standing crop of vege- which the protoplast remains viable for many tative cells (Reynolds et al., 1983b). The success in years. Livingstone and Jaworski (1980)germinated recruiting vegetative cells from excysting propag- akinetes of Anabaena from sediments confidently ules in the following spring is, in part, propor- dated to have been laid down 64 years previously. tional to the abundance of spores retained from On the other hand, rapid akinete production has the previous year (Reynolds, 1978d;Heaneyet al., been stimulated in the laboratory by the sort of 1981). carbon : nitrogen imbalance that occurs as a con- The excystment of vegetative cells from cysts sequence of surface blooming, and from which was firstdescribed by Huber and Nipkow (1922). conditions an effective means of escape is offered Much detail has been added from such land- (Rother and Fay, 1979). Moreover, substantial ger- mark micrographic investigations as those of mination can take place shortly (days rather than Wall and Dale (1968)andChapman et al.(1981). A months or years) after akinete formation, pro- naked flagellate cell, or gymnoceratium, emerges vided the external conditions (temperature, light through an exit slit and soon acquires the distinc- and, possibly, nutrients) are suitable (Rother and tive thecal plates of the vegetative cell. Heaney et Fay, 1977). Reynolds (1972) observed that Anabaena al.(1981)noted a sharp, late-winter recruitment akinetes were regularly resuspended by wind of new, vegetative cells of Ceratium to the plank- action in a shallow lake but failed to germi- ton ofEsthwaite Water, UK, after the water tem- nate before a temperature or insolation thresh- perature exceeded 5 ◦C, and coincident with an old had been surpassed. In other years, vegetative abrupt increase in the proportion of the empty filaments surviving the winter were sufficient to cysts recoverable from the bottom sediments of explain the growth in the following season. These the lake. thresholds could be important to the distribu- Among the Volvocales, sexually produced tions of individual species. The current spread zygotes of (e.g.) Eudorina (Reynolds et al., 1982a) of Cylindrospermopsis raciborskii from the tropics and Volvox (Reynolds, 1983b)havetherobust to continental lakes in the warm temperate belt appearance of resting cysts and, indeed, serve may be delimited by a germination threshold as perennating propagules between population temperature of 22 ◦C(Padisak,´ 1997). The akinetes maxima. Deteriorating environmental conditions of Gloeotrichia echinulata are able to take up phos- may trigger the onset of gametogenesis but for- phate through their walls and colonies germi- mation of the eventual resting stages cannot be nating the following year can sustain substantial claimed certainly to have been consequential on growth even when limnetic supplies are small resource starvation. Among the Chrysophyceae, (Istvanovics´ et al., 1993). there has evolved an opportunistic perennation As suggested above, regenerative strategies are strategy, involving zygotic and asexual cysts that not uniform among the phytoplankton, neither are produced early in the growth cycle, when con- is the production of spores and resting stages ditions are supposedly good (Sandgren, 1988b). exclusively brought on by ‘adverse conditions’. This pattern of encystment apparently ensures However, the existence of resting propagules of theproduction of resting stages during what a given species are likely tolerant of more severe often turn out to be short phases of environmen- conditions than vegetative cells and they do GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 217 increase the probability of survival through diffi- lary of this is that attestably rapid phases of pop- cult times and also perhaps raise the scale of the ulation increase, independent of recruitment by infective inoculum when favourable conditions importation from horizontally adjacent patches return. or from germinating resting stages, are indicative of yet higher simultaneous rates of cell replication. 5.5 Growth of phytoplankton in natural environments Growth rates from episodic events Generically, these accumulative phases fall into two categories. One of these is the annually recur- The rates of cell replication and population rent and broadly reproducible event, such as the growth that are achieved in natural habitats have spring increase of phytoplankton in temperate long been regarded as being difficult to deter- waters, in response to strong seasonally varying mine. This is primarily due to the fact that conditions of insolation (see Section 5.5.2). The what is observable is, at best, a changing den- second is the stochastic event, when, perhaps, a sity of population, expressed as species rate of sharp change in the weather, resulting in the increase (r ,inEq.5.2) which falls short of the n fortuitous stagnation of a eutrophic water col- rate of cell replication because of unquantified umn, or the relaxation from coastal upwelling, dynamic losses of whole cells sustained simul- or the deepening of a nutrient-depleted mixed taneously. The net rate of change can be nega- layer with the entrainment of nutrient-rich met- tive (−r )without necessarily signifying that true n alimnetic water, or some abrupt consumer fail- growth has failed, merely that the magnitude of ure through herbivore mortality, leads to the r ,therateof loss noted in Eq. (5.3), exceeds L realisation of potential respondent growth. In that of replication, r . The problem of patchi- this second category, the phases of increase ness and advection (Section 2.7.2)provides the may be brief and sensing them, accurately and further complication of compounded sampling with reasonable precision, requires the close- errors, in which even the observed rate of popula- interval sampling of well-delimited populations. tion change (±r )mayproveaninadequate base. n The study of in-situ increase rates of phytoplank- From the other direction, the true replication toninBodensee (Lake of Constance), assembled rate cannot be estimated from measurable photo- by Sommer (1981), was one that satisfied these synthetic or nutrient-uptake capacities, unless it conditions. The research based on the large (1630 can be assumed with confidence that the actual m2), limnetic enclosures in Blelham Tarn, English rate of growth is constrained by the capacity fac- Lake District (variously also referred to as ‘Blel- tor concerned. ham Tubes’, ‘Lund Tubes’ (Fig. 5.11), being iso- There are ways around these problems and lated water columns of ∼12–13.5 m in depth and there are now several quite reliable, if somewhat including the bottom sediment from the lake; cumbersome, methods for estimating growth formore details, see Lund and Reynolds (1982), rates in situ. Some of these approaches are high- carried out in the period 1970–84, has similarly lighted below, through the development of an provided many insights into phytoplankton pop- overview of dynamic trait selection in natural ulation dynamics. Examples of specific increase habitats. ratesnoted from either location are included in Table 5.4. 5.5.1 Estimating growth from observations The evident interspecific differences are of natural populations partly attributable to the time period of obser- On the same basis that replication rates cannot vation, and the seasonal changes in water tem- be sustained at a faster rate than cell division can perature and in the insolation attributable to be resourced, it is clear that the observable rates seasonally shifting day length and vertical mix- of population increase cannot exceed the rates of ing. In some instances, these environmental vari- recruitment through cell replication. The corol- ations are reflected in intraspecific variability in 218 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.11 The Blelham Enclosures: the positions of the three butylite cylinders (A, B and C), each measuring about 1630 m2 of water surface and a similar area of bottom sediment, are shown in relation to the bathymetry of the lake. The line X–Y was set up as a permanent transect with shallow (‘S’) and (‘D’) sampling stations. For further details, see Lund and Reynolds (1982).

increase rate. Where species are common to both physiological activity of numerically scarce phy- locations, maximal performances are similar; toplankters are needed to answer this question. species are either fast-growing or slow-growing One of the best-known and most precise tech- in either location. niques for estimating the species-specific growth The observed rates of increase are also plausi- of sub-dominant populations is to estimate the ble in terms of the dynamic behaviours of the frequency of dividing cells. This works best for algae in culture. Allowing for winter tempera- algae whose division is phased (i.e. it occurs at tures and short days, only half of which might certain times of day or night) and it may need be passed in the photic zone, a vernal growth close-interval sampling (every 1–2 h) of the field rate of 0.15 d−1 for Asterionella is perfectly explica- population. It works especially well with algae ble. For small, unicellular species such as Ankyra (e.g. desmids, dinoflagellates, coccolithophorids) and Plagioselmis to be able to double the popu- that have complex external architecture which lation at least once per day in summer (when has to be reproduced at each division and often they can manage it twice in grazer-free, contin- requires several hours to complete. Then the uously illuminated culture) also seems to be a numbers of cells before and after the division reasonable observation. The growth-rate perfor- phase is increased by a number that should agree mances of the bloom-forming Cyanobacteria and with, or be within, the increment deduced from thedinoflagellate Ceratium are about half those thefrequency of dividing cells. Pollingher and noted in culture at 20 ◦C (cf. Table 5.1). Serruya (1976)gavedetails of the application of this method to the seasonal increase of the Frequency of cell division dominant dinoflagellate in Lake Kinneret, now Relatively rapid growth rates, sustained over the called Peridinium gatunense. During the period of equivalent of several cell divisions, lead assuredly its increase (usually February to May), the num- to the establishment of populations making up ber of cells in division on any one occasion was asignificant part of the biomass, if not actu- found to be variable between 1% and 40%. They ally coming to dominate it. It is equally proba- showed that the variability was closely related ble that the same species may be relatively inac- to wind speed. While daily average wind veloci- tive for the quite long periods of their scarcity. ties exceeded 8 m s−1,the frequency of dividing Is their increase prevented by lack of light, or cells (FDC) was always <10%. This accelerated to lack of resources, or losses to grazers, parasites 30–40% during the spring period of weak winds or to the consignment to the depths? Obviously, (and, hence, weak vertical advection) averaging more precise means of investigating the in-situ <3ms−1. Successful recruitment of new cells GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 219

−1 Ta b l e 5.4 Some maximal in-situ ratesofincrease (rn d ) of some species of freshwater phytoplankton reported from Bodensee (Sommer, 1981) and from large limnetic enclosures in Blelham Tarn (Reynolds et al., 1982a;Reynolds, 1986b, 1998b), together with some reconstructed rates of replication (r) where available (see text)

Blelham Enclosure Bodensee a Phase (rn)(rn)(r ) Ankyra judayi MS 0.86 1.09 Plagioselmis nannoplanctica V 0.17 ES 0.56 0.71 Cryptomonas ovata V 0.15 ES 0.46 MS 0.89 0.61 0.62 Dinobryon spp. ES, MS 0.45 0.27 Eudorina unicocca ES 0.43 0.48 Pandorina morum MS 0.52 Coenochloris fottii ES, MS 0.64 0.43 Peridinium cinctum MS 0.18 0.16 Ceratium hirundinella MS 0.17 0.13 Anabaena ﬂos-aquae MS 0.41 0.34 0.34 Aphanizomenon ﬂos-aquae MS 0.43 Microcystis aeruginosa MS 0.24 0.24 Planktotrix mougeotii V 0.06 ES, MS 0.33 0.33 Asterionella formosa V 0.15 0.24 MS 0.36 0.34 0.50 Fragilaria crotonensis V 0.10 MS 0.27 0.24 0.58 LS 0.10 Aulacoseira granulata MS 0.43 Closterium aciculare LS 0.18 Staurastrum pingue LS 0.13 0.28

a ‘Phase’ refers to part of the year: V, vernal, or spring bloom period, temperatures 5 ± 2 ◦C; ES, early-stratification phase (temperature 11 ± 3 ◦C); MS, mid-stratified (temperature 17 ± 3 ◦C); LS, ◦ late-stratified period (temperature generally 12 ± 2 C). divided off at this rate yields maximum rates of reservoir near Madrid to be between 0.13 and population increase equivalent to 0.26–0.34 d−1. 0.16 d−1. More recently, Tsujimura (2003) has The typical net rate of population increase of Peri- estimated in-situ growth rates from FDC among dinium in Kinneret over a sequence of 20 con- cell suspensions of Microcystis aeruginosa and M. secutive years was found to be 0.22 ± 0.03 d−1 wesenbergii from Biwa-Ko (prepared by ultrasoni- (Berman et al., 1992). cation of field-sampled colonies). In both species, Heller (1977)andFrempong (1984)estimated the frequency of diving cells varied between 10% FDC of Ceratium in Esthwaite Water to be between and 15% in offshore stations and between 15% 2% and 10%, occasionally 15%, sufficient to and 40% at inshore stations, with the average explain in-situ seasonal increase rates of 0.09–0.14 duration of cytokinesis varying from 25 h to d−1.AlvarezCobelas et al.(1988)estimatedgrowth 3–6 h. Growth rates of 0.34 d−1 thus appear rates fromafternoon FDC peaks in the popula- sustainable in the near-shore harbour areas of tion of Staurastrum longiradiatum in a eutrophic Biwa-Ko, whence they are liable to become more 220 GROWTH AND REPLICATION OF PHYTOPLANKTON

widely distributed in the circulation of the lake 1996b); just the case of Asterionella formosa in Blel- (Ishikawa et al., 2002). ham Enclosure B in 1978 is highlighted here. The inflatable collar of the enclosure was Frequency of nuclear division lifted on 2 March of that year, isolating part of For phytoplankton species that are less amenable thelake population comprised almost wholly of to the trackingofcelldivision, the principle may Asterionella,then itself already actively increasing, be extended to the monitoring the frequency at a concentration of ∼630 cells mL−1). Over the of karyokinesis (Braunwarth and Sommer, 1985). next 19 days, the population increased exponen- The success of this method relies on the good tially at an average rate of 0.147 d−1,then more fixation of field samples followed by careful slowly to its eventual maximum (a total of 24,780 staining with the DNA-specific fluorchrome, 4,6- cells mL−1,though by then including 1950 cells diamidino-2-phenylindole (DAPI) (Coleman, 1980; mL−1 judged to be dead or moribund) on 4 April. Porter andFeig,1980). This precise and sensi- The decline in the standing population was slow tive method has been applied to a natural Cryp- at first but accelerated enormously as warmer tomonas population (Ojala and Jones, 1993), the and sunnier weather mediated the thermal strat- results being broadly predictable on the basis of ification of the Tarn and the enclosure. Nutrients growth rates under culture conditions. Like any were added to the enclosure each week, by disper- methods based upon the events in the cell cycle, sal into solution across the enclosure surface, in its prospects for measuring replication accurately measured doses respectively designed to restore are high (cf. Chang and Carpenter, 1994). the levels ofavailableresource to 300 µgN,20µg −1 There is also keen interest in sensing the DNA P, 100 µg TFe and 1000 µg SiO2 (466.7 µg Si) L . replication itself. Since the groundbreaking study None of these fell to growth-limiting thresholds. of Dortch et al.(1983), microbial ecolologists have However, there was no artificial relief for either been debating the validity of DNA to cell carbon high pH or probable carbon limitation. The con- as an index of the rate of DNA replication. As an sumption of silicon was calculated as the sum indicator of the capacity for protein synthesis, of the observed decline in the initial concentra- the RNA:DNAratioisalready in use as a barom- tion on 2 March, aggregated with the Si added, eter of the cell growth cycle in marine flagellates and averaged out across the whole volume. The (Carpenter and Chang, 1988;Chang and Carpen- conversion to Asterionella cells between additions ter, 1990)andbacteria (Kemp et al., 1993;Kerkhof was calculated using contemporaneous routine and Ward, 1993). measurements of the Si content of cells sampled from the growing population (consistently within Growth from the depletion of resource therange 51.8–61.1 pg Si cell−1). As there was In contrast to monitoring growth-cycle indica- no other significant diatom ‘sink’ at the time, tors, methods for reconstructing growth rates the consumption was assumed to be equal to from resource consumption are unsophisticated its deposition in new Asterionella frustules. The in approach and notoriously imprecise. However, rate of growth, r (Si),was approximated from the methods invoking uptake of resources deployed numbers of new cells that the observed silicon in specific structures, such as silicon for diatom depletion could have sponsored. Estimates were frustules (Reynolds, 1986a)orsulphur for pro- comparable with the observed rates of increase tein synthesis (Cuhel and Lean, 1987a, b), offer (rn)and with the rates of growth reconstructed more promise. Reynolds and Wiseman (1982) by correcting for the simultaneous loss processes were able to combine the advantages of the spa- (discussed fully in Chapter 6). Simultaneous sink- tial constraints of enclosure, offered by the Blel- ing losses were ‘monitored’ in two ways: using ham tube, with frequent serial sampling of the the flux of settling cells into sediment traps plankton and careful accounting of the amounts placed near the bottom of the enclosure; and of replenishing sodium silicate, in order to mea- using a technique of coring and subsampling sure the true growth rate of a diatom population. thesemi-liquid superficial deposit (see Reynolds, Several datasets were collected and presented 1979a). The possible losses to grazers were esti- (partly also in Reynolds et al., 1982a;Reynolds, mated from contemporaneous measurements of GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 221

Ta b l e 5.5 Comparison of the observed rates of increase in a natural population of Asterionella in a large limnetic enclosure with the growth rate as estimated by silicon uptake. The difference is equated with the rate of loss of live cells (rL) and which may, itelf be compared with simultaneous observations of settling rates (rs) and estimates of the rates of loss to grazers (rg) and to death (rd)

2 Mar–21 Mar 21 Mar–4 Apr 4 Apr–25 Apr 25 Apr–15 May

obs rn 0.147 0.065 −0.032 −0.242 calc rSi 0.154 0.072 0.012 0 calc rL 0.007 0.007 0.044 0.242 obs rs 0.009–0.027 0.016–0.021 0.032–0.126 0.150–0.189 est rg 0.001–0.009 0–0.011 0.001–0.035 0.002–0.040 est rd <0.001 <0.002 <0.031 <0.064 calc r 0.157–0.184 0.081–0.099 0.001–0.160 0–0.051

population, it is possible to calculate a budget for Ta b l e 5.6 Comparison of the observed biomass (as cells per unit area) of Asterionella in Enblosure B, theentire phase of production. These are entered Spring 1978, with reconstructed production (from in Table 5.6,but are calculated for the full water silicon uptake), the total eventually sedimented, the column (mean depth, 11.0 m). The entries are intercepted flux and the estimated loss to grazers at subject to wide margins of error but the agree- the time ment is encouraging: the lower ends of the con-

−9 −2 fidence intervals are mutually compatible. From Cells (10 m ) the aggregate loss of silicon from solution (equiv- −2 Maximum standing crop 272.6 (±19.9) alent to 18.788 g Si m ), the number of Asteri- Production from Si 335.0 (±27.7) onella cells that could have been produced was uptake estimated to have been between 307.3 and 362.7 − Estimated consumption 10.35 (±9.10) × 109 cells m 2.Had they all been in suspen- by grazers sion simultaneously, the concentration would − Sedimentary flux 341.2 (±12.3) have been between 27.94–32.97 × 103 mL 1 (cf. − Recruitment to 319.0 (±58.0) observed maximum, 24.78 × 103 mL 1; 272.6 × sediments 109 cells m−2). The numbers that were recruited to thesediment, the settling flux that was inter- Source: Data of Reynolds and Wiseman cepted and the range of fatalities to grazing are (1982) and Reynolds et al.(1982a), as each inserted in Table 5.6. presented in Reynolds (1996b).

filter-feeding by zooplankton (chiefly of Daphnia 5.5.2 The spring increase in temperate galeata,though activity was minimal until late lakes: the case of Windermere April: Thompson et al., 1982). It is appropriate now to consider an example The various outcomes are tabulated and com- of the role of growth in the development of pared in Table 5.5.Atfirst,almostall the silicon phytoplankton maximum, taking the case of a investment is realised in observable additions familiar and annually recurrent event, observed to the extantpopulation. Moreover the slowing over a sequence of several consecutive years and rate of increase is explained almost wholly by a responding to a substantial degree of interan- declining rate of replication, for whatever reason nual environmental variability. The example of this might be. However, the rates of loss mount the Asterionella-dominated spring increase in Win- and rates of recruitment through cell division dermere is chosen for the length and detail of slow, until the former exceed the latter and the the observational record and because the year- population goes into decline. In this particular to-year variations in the dynamics of growth 222 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.12 The seasonal change in the standing population of live Asterionella cells in the upper 7 m of the South Basin of Windermere (heavy line), averaged over the period 1946 to 1990 inclusive, together with the envelope of 95% confidence (shown by hatching) and the maximal and minimal values recorded (the lighter lines). Modified from an original figure in Maberly et al.(1994) and redrawn with permission from Reynolds (1997a).

and population increase (and subsequent decline) sures, commenced in 1991, see Reynolds and have been intensively analysed. Windermere is a Irish, 2000). By the late 1980s, autumn–winter glacial ribbon lake in the English Lake District, concentrations of MRP increased from a pre-1965 covering 14.76 km2.Itisnotfarshortfrombeing average of 2–2.5 µgPL−1 (0.06–0.08 µM) to ∼8 µg two lakes, a shallow morainic infill separating PL−1 in the North Basin and to about 30 µg thelake into two distinct but contiguous basins. PL−1 in the South Basin. In both basins, autumn– The North Basin holds nearly two-thirds of the winter DIN levels more or less doubled over the total volume (314.5 × 106 m3)andhas a mean same period, from ∼350 to ∼700 µgNL−1 (25– depth of 25.1m(maximumis64m);themean 50 µM), but SRSi levels have remained steady (at −1 −1 depth of the smaller South Basin is 16.8 m (max- 0.9–1.1 mg Si L ; 32–39 µM; 1.9–2.3 mg SiO2 L ). imum 42 m) (data of Ramsbottom, 1976). The This information permits us to establish the southward water flow through the lake is gen- physical–chemical characters of the habitat of erated mainly from the catchment in the central thespring bloom. It is a relatively clear (εwmin uplands of the Lake District. The mean annual ∼ 0.31 m−1)–and soft(alkalinity <0.26 meq L−1) discharge from Windermere (437 × 106 m3 a−1) –water, barely mesotrophic lake, experiencing corresponds to a theoretical mean retention time amostly cool, temperate, oceanic climate, but of 0.72 a. The upper catchment is based upon incurring, between 1965 and 1991, substantial hard and unyielding volcanic rocks, the lower anthropogenic enrichment. For almost 200 years, foothills comprising younger and slightly softer Asterionella has been a conspicuous member of Silurian slates. Both are poor in bases. Thin soils, theplankton in both basins and, during at least mostly cleared of the natural woodland covering thelast 60 of those, the almost unchallenged and replaced with rather poor, leached grazing dominant species of the spring-bloom period. land, contribute little in the way of bases or nutri- Maberly et al.(1994) carried out a thorough ents to the lake. Nutrient loads have increased statistical analysis of the (then) complete run of substantially over the last 50 years or so, through data collected from (mostly) weekly samplings of the increased use of inorganic fertilisers on the the South Basin, initiated by J. W. G. Lund in land. The sheep population that the added fer- 1946 (see Lund, 1949)andmaintained, with only tilty supports has roughly doubled over the same detailed methodological variation, over the 45 period. However, it is the increase in the human years to 1990. A simplified version of their main population, together with the introduction (in figure is reproduced here, as Fig. 5.12,toillus- 1965) of secondary sewage treatment, which has trate the reproducibility of the main features of most affected the phytoplankton-carrying capac- the development. The heavy line represents the ity of Windermere (for full details, reconstructed 45-year mean of the standing population (on a loadings and the effects of the ‘restoration’ mea- logarithmic scale) as a function of the day of GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 223 the year. The narrowness of the 95% confidence general trends over the full period are towards interval (shown by hatching) attests to the strong smaller overwintering inocula but faster rates of interannual comparability of the growth, even exponential rise in the spring. Of particular inter- though the boundaries of the extreme records est is the fact that, although the size of the max- over the 45years(delimited by the lines either imum crop seems not to have increased over the side of the mean plot) cover 2 or more orders 45 years, the date of its attainment has tended to of magnitude of variation. Maberly et al.(1994) be reached earlier in the year, as a consequence of diagnosed several cardinal characteristics of the the trend towards sustained faster growth rates. growth curve, including the size of the extant The maxima of Asterionella in the North Basin population at the beginning of the year (mean of Windermere have been similar in magnitude 9.7 (×/÷ 3.85) cells mL−1;range 0.6–330 mL−1); to those observed in the South Basin in the cor- themaximum (mean 3940 (×/÷ 2.28) cells mL−1 responding years but, typically, have always been range 330–11500 mL−1), the date of its achive- reached one to two weeks later. The greater mean ment (day 124 ± 16.7 (17 April–21 May)), the start depth of the North Basin appeared to be the (day 52 ± 24 (28 January–17 March)) and end most likely reason for this relative delay. However, of the period of rapid exponential increase (day the maxima here are also now reached signifi- 106 ± 17 (30 March–3 May)); the mean rate of cantly earlier (∼10 d) in the year. The proximal increase achieved (0.0925 (± 0.0357) d−1), as well explanation is, again, that a faster average rate as the date of the commencement of the steep of increase is maintained but why this should post-maximum exponential decrease (day 142 ± have changed when light is alleged to be the rate- 16 (6 May–9 June)). regulating factor is not immediately apparent. The source of the bloom is essentially the Circumstantial evidence and some simple standing stock in the water at the turn of the modelling reveal a complex factor interaction at year (Lund, 1949;Reynoldsand Irish, 2000). Inter- work. Starting either from the premise of sus- annual variations in this survivor stock (mean tainable growth rates (Reynolds, 1990)orphoto- 6.6 (×/÷ 4.83) cells mL−1)areinfluenced by the synthetic behaviour (Neale et al., 1991b), it may be size of the late summer maximum of the pre- shown that the long-term average of the under- vious year and the extent of its net dilution by waterlight integral, I∗, sets much lower con- autumnal wash-out. There is a modest increase in straints on Asterionella growth than does water thestanding crop detectable throughout the first temperature, SRSi or SRP concentration. The time few weeks of the year, so thereis,inno sense, track of I∗ in Fig. 5.13 is reconstructed from long- any part of the year when growth is not possi- term (42-year) records of daily integrals of irra- ble. This is close to, or just prior to, the time diance (I0)and wind run, and is hypothesised to of greatest nutrient availability in Windermere, express the intergal daylight period experienced so the restriction on biomass increase has long by entrained algae. Comparison of the modelled been supposed to be physical. The lowest water growth rates, r,asdeterminedbyeachofthe con- temperatures are generally encountered in late straining factors in turn, shows that, initially, the January (days 14–28, weeks 3 or 4, of the year) least are those set by I∗.They move from about but usually remain <7 ◦Cuntilweek 12 (day 84 0.04 to 0.08 d−1 during the first 50 days (7 weeks) and several weeks after the inception of the main of the year, before accelerating up to 0.21 d−1 by exponential increase phase). On the other hand, week 15 (days 98–105). Depending upon the size Talling’s (1957c;seeSection 3.3.3)extrapolations of the starting inoculum, this is sufficient to take of column-integrated photosynthetic production the number of formed cells into the range 103 to in the lake show that light, especially in a fully 104 cells mL− 1 and incipient Si exhaustion. The mixed water column, strongly indicate that light supportive capacity of the initially available sili- is the main growth-regulating factor. The early con is 14–19 × 103 cells mL−1,ifitisassumedthat growth of Asterionella in Windermere has been SRSi is drawn down to extinction and shared at observed to be relatively weak in the stormiest 60–65 pg Si cell−1 produced. Only for the purpose winters predominated by south-westerly winds of modelling is it assumed that there is no con- and stronger inanticyclonic winters. However, comitant loss of cells from suspension, or that 224 GROWTH AND REPLICATION OF PHYTOPLANKTON

there is no demand for silicon from any other agency. In fact, observable populations of 9–10 × 103 Asterionella cells mL−1 will not have formed without using most of the available SRSi, at least down to the critical half-saturation level of 23 µM (see Section 5.4.4). The key deduction is that, prior to 1965, the initially available phosphorus (say 2.5 µgPL−1) would have had to have been shared among a maximal population of 10 × 103 cells mL−1, each having a mean residual quota of ≤2.5 pg cell−1. By halving the quota again, the next cell division will submit the growth rate to P-limitation (see Section 5.4.4). It follows that the diatom- supportive capacity of Windermere is, indeed, set by the available silicon. However, the rate of its assimilation and conversion into Asterionella biomass is closely regulated first by the light income availability but, as soon as this begins to be relieved by lengthening days and weaker vertical mixing, phosphorus availability starts to squeeze the attainable growth rate instead. The final twist in this changing factor interaction comes with the recent phosphorus enrichment of the lake. As first noted by Talling and Heaney (1988), enrichment with phosphorus relieves the growth-rate constraint, which now continues to the limits permitted by I∗, until the ceiling of silicon exhaustion is reached, now rather earlier in the year. The sketches in Fig. 5.14 summarise the shifting date of maximal attainment. The sili- Figure 5.13 Features of the environment of the North con limit remains inviolable. Interactions among Basin of Windermere, during the first half of the year, interannualy varying constraints have influenced influencing the spring increase of Asterionella. The top panel the extent of capacity attainment. Over a num- θ ◦ shows the water temperature ( C), averaged for each week ber of years of enrichment, it became the case of each of 43 consecutive years (1946 to 1988 inclusive, with that the Asterionella maximum failed to exhaust the 95% confidence interval). The second panel shows similar ∗ all the phosphorus in solution, instead leaving it averages for I0, the insolation at the water surface, and for I , the average light level in the mixed layer. Typical (not available tobeexploited by other phytoplankton. statistically averaged) changes in the content of SRSi (soluble As will be argued later (Section 8.3.2), this is a reactive silicon) are shown in the third panel, while the fourth defining stage in the eutrophication of temper- reflects long-term increases in SRP (soluble reactive ate lakes. phosphorus) levels by providing typical trend lines for two There is much more to this story, and to the separate periods (1945–65 and 1980–85). The lower panel next one about the rapid post-maximum collapse θ ∗ shows plots of modelled growth rate capacities of , I , SRSi of the spring bloom. Both concern the magnitude and SRP. The sustainable growth rate is that of the limiting ∗ of the loss terms making up r in Eq. (5.3), discus- component, which, clearly, is I until week 16 or 17, when L diminishing SRP or SRSi levels become critical. Revised from sion of which is developed in Chapter 6.Allthe Reynolds (1990) and redrawn with permission from Reynolds time that the population is increasing, the repli- (1997a). cation rate is sustaining losses of formed cells to mortality – to such physical agents as outwash and settling beyond the resurrecting limits GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 225

behaviour of other kinds of phytoplankton. The main illustrative point is that species have to make the best of the environments in which they find themselves and, often, they must press their specific traits and adaptations to perform adequately under environmental conditions verging on the hostile. In this way, we might interpret the ability of Asterionella to dominate the vernal plankton of Windermere as being dependent upon certain attributes. The first is so obvious that it is easily overlooked: it is there! The success of a species in a habitat is a statement that the habitat is able to fulfil its fundamental survival requirements and, of the species that have arrived there,this species will be, relatively, the most efficient in exploiting the opportunity offered. Absence of a species does not inform a deduction that the habitat is not suitable; it may just not have had the opportunity to grow there. No species dominates a habitat just because theory argues it to be the most suitable. However, to be able to to outperform other species at a given point in space and in time must suggest a favourable combination of inoculum and a rela- Figure 5.14 Reynolds’ (1997b)proposed explanation for tively superior exploitative efficiency under the the advancing date of the Asterionella maximum in conditions obtaining. Windermere. (a) On the plot of accelerating standing crop, The fossil record shows that Asterionella domi- the ceiling capacity of the silicon resource K(Si) occurs only a nance is a relatively new phenomenon in Winder- little short of the point where the supportive capacity of the mere, having occurred only since the nineteenth phosphorus would have been exhausted, although recent century (Pennington, 1943, 1947). Previously, phosphorus enrichment has raised this ceiling further. Thus in Cyclotella species had dominated a more olig- (b), the likelihood of a phosphorus-limited growth rate is otrophic period in the lake’s history (Haworth, delayed and relatively fast growth rates can be maintained for longer. The silicon ceiling, which has remained stable, is thus 1976). Asterionella is able to grow faster than other reached sooner. Changing nutrient availability may be cited diatoms under the poor vernal underwater light for the advance which may have little or nothing to do with conditions and faster than Planktothrix at low climate change. Redrawn with permission from Reynolds temperatures. It also manages to carry over sub- (1997b). stantial winter populations from which spring growths can expand. Asterionella does not have of entrainment and to the biological demands matters exclusively to itself – Aulacoseira species of grazing and parasitic consumers. The spring (A. subarctica, A. islandica)overwinter well, though bloom in Windermere, as elsewhere, is sustained they grow less rapidlythan Asterionella; flagellates to within the limits that light and available nutri- such as Plagioselmis grow relatively well in win- ents can support, net of ongoing sinks, recognis- teranticyclones (with frosts, sunshine and weak ing that the latter may be more or less critical in wind-driven vertical mixing) (Reynolds and Irish, commuting the size of the maximum crop below 2000). that of the chemical capacity. Small interannual variations in these environ- 5.5.3 Selection by performance mental features may not make decisive intrasys- The example of Asterionella in Windermere may, tem differences in outcomes but they may assist or may not, have direct analogues to other us to understand the differences in timing, the diatom blooms in other systems or even to the magnitude of crops and the species dominance of 226 GROWTH AND REPLICATION OF PHYTOPLANKTON

populations elsewhere. We have shown, through dence between 18 and 20 ◦C. There also seems the comparison of growth responses and their to be a common threshold light exposure (∼4h sensitivities to environmental deficiencies, how d−1 on the analogue scale) applying at all tem- the dynamic performances differ among species peratures. The information sits comfortably with in experiments. Can we now discern differences our understanding of growth sensitivites in the of performance in nature that will confirm – laboratory. It may also be noted that the repli- or help us to recognise – the traits that select cation rates in the field do not differ widely for somespeciesand against others at a given from the maximum resource- and light-saturated location? If so, how much does this tell us about rates observed in culture at 20 ◦C, if the appro- thewaysinwhich natural communities are put priate adjustments for temperature and photope- together and shape trophic relationships? riod are applied. The answers to these questions are clouded Analogous deductions can be drawn from the by theusual problems of accurate measure- data for the other algae represented in Fig. 5.15. ment of population dynamics in the field (see The ability of another R-strategist alga, Asteri- Section 5.5.1). Work with captive wild popula- onella,toadapt to function on low average insola- tions of phytoplankton in the Blelham enclo- tion is confirmed by observed growth rates of up sures, growing within a defined space, subject to 0.15 d−1 on a low aggregate daily photoperiods to well-characterised and, in part, artificially con- (≤4hd−1 on the contrived scale) at temperatures trolled conditions, subject to separately quanti- from 5 to15◦C. Collected data for Cryptomonas fied loss rates of cell loss and, above all, sam- spp. (mostly C. ovata) and Planktothrix mougeotii pled at high frequencies (3–4 days), does provide also confirm that growth rates are maintained some insights. From data collected from numer- by photoadaptation to low aggregate insolation ous growth phases, observed in three enclosures (with thresholds of 1–3 h d−1) but they are not over 6 years, Reynolds (1986b)assembled a series so fast as the most rapid performances of the of in-situ replication rates for each of a number diatoms. The most rapid growth rates observed in of common species. Summaries are shown in Fig. theenclosures have been attained by C-strategists 5.15. Each datum point is calculated from a mini- such as Ankyra, which, on several occasions, has mum of three serial measurements on an increas- been observed to self-replicate at >0.8 d−1 (dou- ing population and is corrected for the contem- bling its mass in less than a day!). These short- poraneous estimates of loss rates to sinking and lived episodes have been possible in warm, clear, grazing (details to be highlighted in Chapter 6). usually water that is restratifying and supplied These points were then plotted against a common with nutrients well in excess of growth-rate lim- scale of analogous insolation, this being the prod- iting concentrations. Lack of carbon, self-shading uct of the day length (,fromsunrise to sunset, or increased vertical mixing contribute to a slow- in hours) and the ambient ratio of Secchi-disk ing growth rate in these instances: note the −1 depth to mixed depth (zs/zm,withtheproviso apparent threshold at ∼8hd on the contrived that solutions >1aretreatedas1). Finally, the scale of daily photoperiod. The plots for the C–S points are grouped according to the approximate species Eudorina unicocca seem to point to an even contemporaneous water temperatures. greater photoperiod response, little influenced The plot does reveal an encouraging level by the(somewhat narrow range of) water tem- of intraspecific consistency of performance and peratures available. The two strongly S-strategist significant interspecific differentiation. Taking Cyanobacteria (Anabaena and Microcystis)aregen- the observations on Fragilaria,forinstance, erally slow-growing (<0.36 d−1); as a function of replication rates in the field, between 13 and photoperiod, there is an intermediate threshold 17 ◦C, reveal a common dependence upon the of 4–6 h d−1 on the artificial scale. aggregate-by-analogy photoperiod, with a slope Many other observations on the growth per- that appears steeper than (two) observations formances of phytoplankton have emerged from applying to temperatures between 9 and 11 ◦C, yet thestudies using the Blelham enclosures. Some less steep that the indicated photoperiod depen- relate to the dynamics of loss and the way these GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 227

Figure 5.15 Approximations of the daily specific growth interact with differential growth rates in influ- rates (r = r + r + r )reconstructed from detailed n G S encing community assembly and succession, to observations on the dynamics of populations of named phytoplankters in Blelham enclosures, plotted against the which reference will be made in subsequent contemporaneous products of the length of the daylight chapters. Of particular interest to the question period (,inh)and the ratio of the Secchi-disk depth to the of selection by growth performances is the ∗ mixed depth (hs/hm), being an analogue of I (in instances collective overview of species-specific devel- where hs/hm > 1, hs/hm is put equal to 1). Curves are fitted opment in relation to chemical factors. The to data blocked according to contemporaneous enclosures have been subject to differing levels temperatures, as stated. The algae are: Anaba, Anabaena of fertilisation, and to variation in the frequency flos-aquae; Ankyr, Ankyra judayi; Aster, Asterionella formosa; and the scale of nutrient supplied. Against Crypt, Cryptomonas ovata; Eudor, Eudorina unicocca; Fragi, thenaturally soft-water, relatively P-deficient Fragilaria crotonensis; Micro, Microcystis aeruginosa; Plank, Planktothrix mougeotii. Modified and redrawn with permission water of Blelham Tarn, it is not surprising from Reynolds (1986b). that manipulations of the phosphorus and the carbon content of the enclosed water should have yielded the most satisfying outcomes. Reynolds (1986b) contrasted the yield of phytoplankton, in terms of biomass and species composition, through six enclosure–seasons 228 GROWTH AND REPLICATION OF PHYTOPLANKTON

Urogl/Dinob Aster Eudor subject to P loads between 0.3 and 2.5 g P 6 m−2. Many species occurred in all sequences but in differing absolute and real proportions. Some were relatively much more frequent at 0 high rates of P fertility and some were rela- Coeno Plank Ankyr 6 tively more abundant at low rates. Using more enclosure-years (making 18 in total) but in lesser detail and in respect of a small number of repre- 0 sentative species, Reynolds (1986b)summarised Anaba Crypt Staur the apparentpreferencesofcertain speciﬁc 6 ascendencies to reveal the patterns shown in Fig. 5.16. Whereas Asterionella dominated for a time in every enclosure in every year and the inci- 0 dence of dominant populations of Planktothrix, Cerat Fragi Micro 6 Cryptomonas, Fragilaria and Microcystis was not clearly correlated with the eightfold variations in phosphorus supplied, the growth of Eudo- 0 rina, Ankyra and the desmid Staurastrum pingue showed preferences for phosphorus richness. On 1.02.0 1.0 2.0 1.0 2.0 P loa / g P m−2 theother hand, the chrysophytes Uroglena and Dinobryon,aswell as the colonial chlorophyte Figure 5.16 The frequency of years (out of 18) in which Coenochloris, conformed to supposition (Table 5.2) the annual areal load of phosphorus added to a Blelham by ﬂourishing well down the scale of phosphorus enclosure fell within the ranges stated (0–0.5, 0.5–1.0 g P fertility. Population development of Anabaena −2 m , etc.) and the number of years in each category during and Ceratium also shows bias towards the less which the named phytoplankters produced a dominant or enriched conditions. large sub-dominant population. Species abbreviations as in Fig. Following a similar approach, increase phases 5.15, plus: Cerat, Ceratium hirundinella; Coeno, Coenochloris fottii; Dinob, Dinobryon spp.; Staur, Staurastrum pingue; Urogl, Uroglena of the same group of species were blocked as a cf. lindii. Redrawn with permission from Reynolds (1986b). function of the pH of the water in which they grew (see Fig. 5.17). The water in Blelham Tarn has a rather low bicarbonate alkalinity (<0.4 meq L−1)and, in the enclosures, it is isolated from

4 Urogl/Dinob Eudor 12 Figure 5.17 The frequencies with which the increase phases of Aster 8 dominant phytoplankton species in the Blelham enclosures were halted in the pH ranges indicated (pH Volvo 2 Plank 4 7.0–7.5, 7.5–8.0, etc). Species Ankyr 2 abbreviations as in Figs. 5.15 and 2 Coeno 4 Cerat 5.16, plus: Coeno, Coenochloris fottii. Anaba 4 Redrawn with permission from Fragi 4 Reynolds (1986b). Micro 4 Crypt 8 4 Staur 0 0 7 8 9 10 11 7 8 9 10 11 pH pH GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 229

Figure 5.18 Simultaneous changes in the concentrations of vegetative cells of the dinoflagellate Ceratium hirundinella in the Blelham Enclosures A, B and C, during 1980. Cyst production, noted in the figure, generally marks the termination of vegetative growth. Redrawn with permission from Lund and Reynolds (1982). terrestrial replenishment (Fig. 5.11). Thus, the organism so much as those of them that were inorganic carbon supply to phytoplankton in there were able to contend effectively with the these experiments depended upon internal recy- conditions imposed. Yet, in many ways, these rela- cling, augmented by whatever dissolved from the tive performances do, most probably, distinguish air at the water surface. Thus, rising pH is a use- sufficiently among the traits and adaptabilities ful surrogate of carbon deficiency in the enclo- of a number of common types of plankter for sures (experiments in 1978 attempted to relieve their basic ecological preferences and sensitivi- thedeficiency with additions of bicarbonate; they ties to be recognised and identified in further, did increase carbon but did not reduce pH). The more focussed testing. species-specific distributions of histograms in Fig. We see that enrichment with nutrient seems 5.17 peak in range 9.0–9.5, simply because that is to be beneficial to most species, raising the ceil- also the range reached most frequently during ing of attainable biomass and, in many instances, themaxima encouraged by fertiliser additions; releasing the growth rate from the restriction it is not necessarily indicative of any algal pref- of nutrients. This may not be universally so, erence for this range. However, it is evident that forsome of the inherently slow-growing, self- Fragilaria, Cryptomonas, Eudorina, Ankyra, Ceratium regulating species, like Ceratium hirundinella,have and, especially, Anabaena, Microcystis and Stauras- adaptations for supporting their growth require- trum pingue were all ablealltofunction at pH ments under nutrient-segregated conditions and levels up to 1 point higher. The observation growth rate is not necessarily enhanced by nutri- matches those of Talling (1976) concerning dif- ent abundance. The growth-rate performances ferential insensitivity to carbon dioxide shortage; achieved by Ceratium in each of the three enclo- all these species are known orsuspected for the sures during 1980 were ultimately comparable efficiency of their carbon-concentration mecha- (see Fig. 5.18: 0.092 d−1 in Enclosure A, 0.098 d−1 nisms (Section 3.4.3). The apparent failure of the in Enclosure B and 0.105 d−1 in Enclosure C), even chrysophytes Uroglena and Dinobryon to maintain though the non-physical growth conditions were growth at pH levels ≤9aroused the suspicion quite disparate. That the yields were quite differ- that these algae might be obligate users of carbon ent is influenced by the length of time that cell dioxide (Reynolds, 1986b), as indeed, has since division was maintained in situ. This was partly been verified in the laboratory (Saxby-Rouen et al., influenced by resource availability and, as is now 1998). known, by resource renewal in the graded Enclo- These response patterns require careful inter- sure C (Fig. 5.11;Reynolds, 1996b). The major pretation and their subjectivity to the experi- influence, however, is the source of excysting mental design must be taken into account. The inocula. The uniformly deep sediments of Enclo- species responding to the conditions contrived sures A and B supported many fewer surviving are, almost exclusively, the ones that are already cysts than those of Enclosure C, whereas recruit- well established in the lake and/or the exper- ment of ‘germinating’ gymnoceratia (see Section imental enclosures. The observed performances 5.4.6)was also relatively stronger in Enclosure are not necessarily those of the nature’s ‘best-fit’ C. It is interesting, indeed, that Lund (1978) had 230 GROWTH AND REPLICATION OF PHYTOPLANKTON

Figure 5.19 The maximum fraction of the summer standing phytoplankton biomass in Blelham enclosures contributed by nitrogen-ﬁxing species of Anabaena and Aphanizomenon in each enclosure–year, plotted against the corresponding areal loading rates of nitrogen and phosphorus. Their relative abundance generally coincides with low nitrogen and moderate phosphorus availability but not onalowN:Pratio per se. Redrawn with permission from Reynolds (1986b).

regarded the enclosures as being somehow hos- sus P fieldofFig.5.19, corresponding to load- tile to Ceratium,forthealgahad never become ings of 6–10 g N m−2 (0.45–0.71 mol m−2)and so numerous as in the lake outside. As Fig. 5.18 0.19–1.2 g P m−2 (6–38 mmol m−2), but with no demonstrates, there is nothing about these enclo- cleardependenceonN:P(actual ratios 12–118). sures that interferes with growth. Isolation of At higher loads of N and P (but with ratios still the water from that of the lake, except during in the order of 10–20), the species were hardly winter opening, evidently made it difficult for represented at all. Thus seasonal dominance by Ceratium to invade in numbers. The point about these species has failed to come about under Enclosure C is that the presence of shallow sed- conditions in which neither nitrogen nor phos- iments assisted the success of perennation and phorus was likely to have been limiting plankton reinfection of the water column in the spring. growth. What can be said is that, at the low nitro- This pertinent biological observation was, obvi- gen concentrations limiting non-N-fixing species, ously, quite peripheral to the design and purpose the yields of Anabaena and Aphanizomenon are of the experiment. broadly proportional to phosphorus loadings up The behaviour of Anabaena,asupposed indi- to ∼1g(or ∼30 mmol) P m−2.Athigher levels cator of carbon-deficient eutrophic waters, and of N and P, there will always befaster-growing its apparent preference for less-enriched condi- species – such as Ankyra, Chlorella, Plagioselmis, tions may also be explained from more detailed Cryptomonas,evenEudorina –poised to outper- analysis. Suspecting a performance influenced form them. by the ratio of available nitrogen to available Finally, additional information is available phosphorus, the maximum fractional abundance from the enclosure work to amplify the specific of Anabaena spp. (plus the smaller amounts of growth performances under persistent and rela- Aphanizomenon)inanygivenenclosure year was tively low phosphorus concentrations. Coenochlor- plotted against the coordinates of the nitrogen is fottii featured prominently in a number of and phosphorus supplied (Fig. 5.19). Anabaena thesequences (it was then referred to Sphaero- spp. featured in most annual sequences observed cystis schroeteri). It was relatively more common in the enclosures but only occasionally did it in the summer periods when phosphorus was produce dominant populations. Moreover, when strongly regulating biomass and growth (see levels of DIN had fallen much below 100 µg especially Reynolds et al., 1985)butabsolutely Nl−1 (∼7 µM), populations developed substan- larger populations and sustained growth rates tial heterocyst frequencies (maximum, 7% of were observed at greater nutrient availabilities all cells). In terms of N and P loads, how- (Reynolds et al., 1983b, 1984). With the impos- ever, Anabaena and Aphanizomenon abundances ition of artificial mixing, the alga was again are clustered within one corner of the N ver- found to be tolerant but only for so long as GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 231 thewater was clear and the ratio of Secchi- disk depth to mixed depth (zs/zm)wasnear or greater than 1. Noting rather smaller numbers of Oocystis aff. lacustris, Coenococcus, Crucigeniella and the tetrasporalean Pseudosphaerocystis lacustris (formerly Gemellicystis neglecta)showed similar responses to imposed variations in nutrients and insolation, Reynolds (1988a)grouped all these non-motile, mucilaginous colonial Chloro- phyceae in a single morphological–functional group of non-motile, light-sensitive, mucilage- bound species. It is their behavioural traits with Figure 5.20 Differing demographic behaviours in respect to threshold light levels that tend to exploiting favourable growth opportunities: species grow exclude them from turbid or deep-mixed water either rapidly and invasively (1) or more slowly to build a columns and to give them a common association conserved, acquisitive population (2). Slow accumulation of with oligotrophic lakes. For the common chrys- biomass may be offset by the recruitment of pre-formed propagules from a perennial seed bank (3). Modified after ophyte species of Dinobryon, Synura and Uroglena, Reynolds (1997a). the apparently similar association with nutrient poverty in the enclosures is not due to any intol- erance of high nutrients but to an unrelieved higher-biomass-achieving K-selected trait of many dependence upon the supply of carbon dioxide, larger algae, represented by Curve 2 in Fig. 5.20, which, in the soft-water confines of the Blelham which, initially, lags behind the performance of enclosures, is readily outstripped by demand more r-selected species (Curve 1) is characteris- (Saxby-Rouen et al., 1998). tic of the performances of S- and CS-strategists. However, it is also clear that some of the self- 5.5.4 Temporal changes in performance regulating S-strategists, such as Ceratium and selection Microcystis,are obliged to grow so relatively slowly There is clearly a good match between how the that eventual abundance in the plankton is influ- various species studied in the controlled field enced by the recruitment of sufficient peren- conditions of the Blelham enclosures and the nating propagules at the initiation of the next sorts of trait characteristics and strategic adapta- period of growth. This very strong K-selected fea- tions identifiable among the properties revealed ture is represented by Curve 3 in Fig. 5.20. in earlier sections (especially pp. 31–34). In par- We may venture further than this by superim- ticular, a distinction is to be made between the posing the triangular ordination of species traits manner in which species develop their popula- (e.g. of Fig. 5.9)and overlaying this on a notional tions in response to what are perceived by them plot to describe the interaction of mixing and to be favourable conditions. On the one hand, nutrient availability in the near-surface waters there are species that specialise in rapid, inva- (see Fig. 5.21). The loops and arrows are inserted sive growth, building up stocks at the expense to show how temporal seasonal variations in the of freely available resources and high photon coordinates of nutrient availability and mixing fluxes, and which, by analogy to the terminol- might select for particular performances and rel- ogy of Grime (1979, 2001), we have defined r- evant traits and adaptations. These are notional selected C-strategists (see Box 5.1). Besides the and unquantified at this stage of the develop- examples of Ankyra and Chlorella, Asterionella and ment and the representation is qualitative but some of the other freshwater diatoms that are they illustrate some general points that need to tolerant of intermittent and poor average inso- be made. The two large loops (marked a and b) lation (R-strategist traits) are also strongly r- reflect the transitions that might be observed selected over other R-type species such as Plankto- over a year in a seasonally stratified (not nec- thrix agardhii. The slower growth but often essarily temperate) lake. At overturn, there is a 232 GROWTH AND REPLICATION OF PHYTOPLANKTON

at the extremes. The converse is that variability is good for maintaining high diversity as more specific performances are accommodated. The constrained cycles of (say) an enriched water column subject to variable stratification or of persistently mixed, resource-cycling systems may also be represented in this scheme (respectively, c and d). Other factors notwithstanding, the effects of population growth should follow the direction of the arrow (marked e) as nutrients are withdrawn from the water and the increasing biomass reduces light penetration and the relative mixed depth is increased. The traces provide adequate summaries of changes in seasonal dominance in given lakes and, to an extent, they may reflect longer- Figure 5.21 Notional representation of Grime’s CSR triangle on axes representing relative nutrient abundance and term changes in phytoplankton inresponse to water-column mixing, showing the adaptive traits most likely nutrient enrichment or restoration measures. to be selected by changing environmental conditions. The In the naturally eutrophic, nutrient- and base- loops represent time tracks of selective pressures acting rich kataglacial lakes of northern Europe and through the year in (a) oligotrophic lakes, (b) eutrophic lakes, North America (see, for instance, Nauwerck, 1963; (c) and (d) in smaller, enriched systems; (e) is the anticipated Lin, 1972;Kling, 1975;Reynolds, 1980a), the course of autogenic succession. Redrawn from Reynolds annual cycle of phytoplankton dominance fea- (1988a). tures (i) vernal diatoms (which may include any or all of Asterionella formosa, Fragilaria crotonen- rapid rightward shift on the mixing axis with sis, Stephanodiscus rotula, Aulacoseira ambigua from an upward drift as dissolved nutrients are redis- the R apex of the triangle), followed by (ii) a persed from depth. The best-performing species burst of readily grazeable, plainly C-strategist here and throughout the bloom period are likely nanoplankton (e.g. chlorellids, Ankyra, Chlamy- also to show the traits and growth responses of R- domonas, Plagioselmis), and/or (iii) by populations strategist species: the limits of their morphologi- of colonial Volvocales (e.g. Eudorina, Pandorina – cal and behavioural adaptations are more suited best classed as CS strategists) and increasingly to coping with low average insolation. The onset more S-strategist Anabaena spp., Microcystis or Cer- of themal stratification is represented by a lurch atium). The cycle is completed by (iv) assemblages to the left, where conditions of low relative mix- of diatoms (Fragilaria, Aulacoseira granulata)and ing and high relative nutrients obtain and which, desmids (Closterium aciculare and several species of initially, are open to exploitation by fast-growing Staurastrum). C-strategist species. Their activity depletes the In the nutrient- and base-deficient lakes of resources and may lead, eventually, to the par- theEnglish Lake District (Pearsall, 1932), the titioning of availability and to the dependence oligotrophic subalpine lakes of Carinthia (Find- upon increasingly effective S-strategist adapta- enegg, 1943)and the more oligotrophic lakes of tions to access them. Note that the more severe NewYork and Connecticut studied by Huszar and ongoing is the insolation or resource defi- and Caraco (1998), as well, in all probability, ciency, the closer are the trajectories to the apices similar lakes throughout the temperate regions of the CSR triangle, where the relevant adapta- (Reynolds, 1984a, b), the vernal plankton is typ- tions become ever more important. As a conse- ically dominated by Cyclotella–Urosolenia diatom quence, the few that have them are alone able to associations (R or CR strategists). These may be perform successfully at all. The potential diver- replaced typically by such chrysophytes as Dino- sity of surviving species is finally ‘squeezed out’ bryon, Mallomonas or Synura (RS strategists) and/or GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 233 by colonial Chlorophyceae (CS strategists), then within 4–6 months before being short-cut back by S-strategist dinoflagellates (Peridinium umbon- to an earlier stage. Even in temperate lakes and atum, P. willei or Ceratium spp.) and, finally, by R or reservoirs subject to extreme fluctuations in SR desmids such as Cosmarium and Staurodesmus. mixed depth on scales of 5–50 days, alternations Between the oligotrophic and eutrophic sys- between phases of increase and dominance tems are ranged the lakes of intermediate sta- by R species (Stephanodiscus, Synedra)andC–S tus (mesotrophic lakes), as well as several deep groupings (cryptomonads, Chlamydomonas, Oocys- alpine lakes of central Europe (Sommer, 1986; tis, Aphanizomenon)are clearly distinguishable Salmaso, 2000; Morabito et al., 2002)Here, the ver- (Haffner et al., 1980;Ferguson and Harper, nal phase is characterised by R-strategist diatoms 1982). Again, in nutrient-rich lakes where the featuring perhaps Aulacoseira islandica or A. sub- alternations result in the lake being either arctica,aswell, perhaps, as Asterionella, Fragi- predominantly mixed or stratified, so the dom- laria or Cyclotella radiosa. There is a late-spring inating species would be (respectively) R species phase of C strategists (e.g. Plagioselmis, Chrysochro- (as in Embalse Rapel, Chile: Cabrera et al., 1977) mulina), followed either by a phase of colo- or C species (as in Montezuma Well, Arizona: nial Chlorophyceae–Chrysophyceae or, especially Boucher et al., 1984). These possibilities comply in deeper lakes, S-strategist Ceratium or Peri- with the track marked (c) in Fig. 5.21.Examples dinium,orbytheCyanobacteria Gomphosphaeria of enriched shallow or exposed lakes that are or Woronichinia,oragainperhaps by potentially more or less continuously mixed seem to be dom- nitrogen-fixing Anabaena solitaria, A. lemmerman- inated by the K-selected R strategists (Planktotrix nii or Aphanizomenon gracile.Late-summer mixing agardhii, Limnothrix redekei, Pseudanabaena spp.: may favour R-strategist diatoms (notably includ- Gibson et al., 1971;Berger,1984, 1989;Reynolds, ing Tabellaria flocculosa or T. fenestrata), desmids or 1994b)arerepresented in Fig. 5.21 by track (d). the filamentous non-diatoms (such as Mougeotia, It is not yet possible to apply the same Binuclearia, Geminella). The outstanding algae of approach to temporal changes in the marine the deepmesotrophic systems, however, are the phytoplankton with a similar level of inves- RS-strategist Planktothrix rubescens/mougeotii group tigative evidence, as the resolution of temporal which both tolerate winter mixing and exploit changes is less clear. On the other hand, it is deep stratified layers in summer. atestable hypothesis that similar performance- The cycles in Fig. 5.21 are not tracked at an led drivers, influenced by similar morpholog- even rate, neither are they precisely identical ical adaptations to analogous liqiud environ- each year. Progress may proceed by a series ments, govern the spatial and temporal differ- of lurches, whereas interannual variability can ences in the growth of phytoplankton in the divert the sequence to differing extents. However, sea. There is good supporting evidence that this the growthandpotential dominance of phyto- may be the case. Smayda (2000, 2002) has shown plankton adheres closely to the model tracking that the wide diversity among the dinoflagel- (Reynolds and Reynolds, 1985). The cycle may be lates may be rationalised against an ecological completed in less than a year: the description of pattern that invokes morphology. Whereas the Berman et al.(1992)oftheperiodicity of phyto- smaller, non-armoured adinophytes (such as Pro- plankton of Lake Kinneret follows a mesotrophic rocentrum) and gymnodinioids (Gymnodinium, Gyro- path before stalling in summer deep on the left- dinium, Heterocapsa spp.) that are characteristic of hand (nutrient) axis of Fig. 5.21.Itdoesnot really shallow, enriched coastal waters have unmistake- move on until wind-driven mixing or autumn ably C-like morphologies and growth-rate poten- rains relieve the severe nutrient (nitrogen and tial, the larger, armoured and highly motile cera- phosphorus) deficiency. The cycle may also be tians have clear S tendencies. In the open ocean, recapitulated: Lewis’ (1978a) detailed description Smayda (2002)distinguishes among dinoflagel- of the seasonal changes in the plankton of Lake lates associated preferentially with fronts and Lanao, Philippines, could reasonably represented upwellings (Alexandrium, Karenia)andthoseof by track (b) in Fig. 5.21 but it would be completed post-upwelling relaxation waters (Gymnodinium 234 GROWTH AND REPLICATION OF PHYTOPLANKTON

catenatum, Lingulodinium polyedrum). S-strategist supreme over vast areas of ultraoligotrophic dinoflagellates are also prominent in the oligo- ocean, as archetypes of the newly proposed SS trophic, stratified tropical oceanic flora, where strategy. self-regulation, high motility and photoadapta- Seasonal changes in the plankton flora of tive capabilities distinguish such dinoflagellates theEnglish Channel, described by Holligan and as Amphisolenia and Ornithocercus. The buoyancy- Harbour (1977), show a clear tendency for ver- regulating adinophytes of the genus Pyrocystis are nal diatom–dominated (supposedly R-strategist) most remarkable in showing parallel adaptations assemblages to be displaced by more mixed to limnetic Planktothrix rubescens and insimilarly diatom-dinoflagellate (CR?) associations (Rhizosol- constituting a mid-water shade flora, deep in the enia spp.; Gyrodinium, Heterocapsa, Prorocentrum)in light gradient of the tropical ocean. early summer and by green flagellates (Carteria, It is interesting to speculate on the range Dunaliella, Nannochloris)or(S?) ceratians (Ceratium of adaptations among the planktic diatoms of fusus, C. tripos)inmidtolate summer. In enriched the sea. Most are non-motile and (presumably) near-shore areas, the haptophyte Phaeocystis,in reliant upon vertical mixing for residence in its colonial life-history stage, may dominate the the near-surface waters. Thalassiosira nordenski- early summer succession, in a manner strongly oldii, Chaetoceros compressus and Skeletonema cost- reminiscent of the abundance of volvocalean CS atum are all chain-forming diatoms featuring strategists in eutrophic lakes. in the spring blooms of North Atlantic shelf Asatisfying aspect of the performances of waters. The attenuate forms of species of Rhizosol- phytoplankton in both the sea and fresh waters is enia, Cerataulina, Nitzschia and Asterionella japonica thesuperior influence of morphological and (pre- are conspicuous in the neritic areas. All these sumably) physiological criteria over phylogenetic diatoms can be accommodated in the under- affinities. This is a powerful statement attest- standing of R-strategist ecologies. However, there ing to evolutionary adaptations for relatively spe- are also centric diatoms such as Cyclotella capsia cialised lifestyles and for the radiative potential that occur predominantly in shallow eutrophic latent within all major phyletic divisions of the coastal waters and estuarine areas, along with, photosynthetic microorganisms. arguably, C-strategist green algae (Dunaliella, Nannochloris), cryptomonads, the dinoflagellate 5.5.5 Modelling growth rates in field Prorocentrum,theeuglenoid Eutreptia and the There has for long been a requirement for robust, haptophytes Chrysochromulina and Isochrysis.In predictive models of phytoplankton. Nowadays, another direction of adaptive radiation, the very theelement of stochasticity of environmental large, self-regulating Ethmodiscus rex,belonging to events is appreciated as a near-insuperable bar to thetropical shade flora, shows the typical prop- accurate predictions of sufficient precision. How- erties of an S-strategist species. ever, considerable use can be made of the regres- Many coccolithophorids are small and are sions fitted to growth performances in the labora- regarded, somewhat ‘uncritically’ (Raymont, tory and the philosophy of strategic adaptations 1980), as nanoplankton. Emiliana huxleyi, Gephyro- to drive predictive solutions to which of certain capsa oceanica and Cyclococcolithus fragilis are, kinds of alga will grow in particular water bodies indeed, small C-like species of open water, and under which conditions. which they inhabit with nanoplanktic flagel- This section is not intended to provide a guide lates, including the prasinophyte Micromonas, or a review of different modelling approaches. the chlorophytes Carteria and Nannochloris,the These are available elsewhere (Jørgensen, 1995, cryptophytes Hemiselmis and Rhodomonas and 1999). The purpose here is to refer to some of the haptophytes Pavlova and Isochrysis. The theapproaches addressed specifically to mod- nitrogen-fixing, vertically migrating Cyanobac- elling growth and performance of phytoplank- terium Trichodesmium displays strong S-strategist tonand to promote the use of models that characteristics. The picoplanktic Cyanobacteria invoke them. It is worth first repeating the obvi- Synechococcus and, especially, Prochlorococcus,reign ous, however, that different models attempt to GROWTH OF PHYTOPLANKTON IN NATURAL ENVIRONMENTS 235 do different things. These may be in-and-out uously overrides the others. This was the case in ‘black-box functions’, such as Eq. (4.15), where an the models of growth of filamentous Cyanobac- input (in this case, biologically available phos- teria in an enriched, monomictic lake (Jiménez phorus) generates a yield (in this case, phyto- Montealegre et al., 1995)ordeep in the light plankton chlorophyll) on the basis of pragmatic gradient of the Zurichsee¨ (Bright and Walsby, observation, without any attention to the explica- 2000). A most promising modern development tive processes. These internal linkages may be has come through the exploration of linkages investigated, imitated and submitted to empiri- (stimulus, responses) and the probabilistic analy- cal model explanations, for instance, those which sis of effects (likely reaction) through artificial link the generation of phytoplankton biomass neural networks (ANNs) (see Recknagel et al., to photosynthetic behaviour in the underwater 1997). Like the nerve connectivities they resem- light field. The various explanative equations of ble, these models can be ‘trained’ against real (say) Smith (1936), Talling (1957c), Pahl-Wostl and data in order to predict outcomes with modi- Imboden (1990)predict, with accuracy, precision fied variables. Recknagel’s (1997)own application and increasing detail, the photosynthetic car- to interpret the variability in the phytoplank- bon yield as a function of light and respiration. ton periodicity in Kasumigaura-Ko in Japan pro- They are, nevertheless, restricted in their effec- vides an excellent indication of the power of this tiveness to cases where anabolic processes are approach. Its further development is at an early simultaneously constrained by some other fac- stage but the use of ‘supervised’ and ‘unsuper- tor (carbon or nutrient supply). What is then vised’ learning algorithms to interpret field data, needed is the further sets of precisely quan- through ‘self-organising maps’ of close interre- tifiable algorithms that will describe these fur- lationships (Park et al., 2003), promises to over- ther processes (many of which are available) and come some of the difficulties experienced with their incorporation into a supermodel to simu- other compound models. Prediction of ‘top-line’ late the interactions among all the components. outcomes based on ‘bottom-line’ capacities is gen- In a third type of model, the broad function of erally difficult without knowledge of interme- thesystem (‘the box’) is predicted from a knowl- diate processes. The fundamental truth is that edge of the fundamental mechanisms and limi- algal growth rate is not a continuous function tations (such as genomic information and energy of nutrient supply or uptake, or of the ability to efficiency), as elegantly employed in Jørgensen’s fix carbon in the light. Below the ‘threshold’ val- (1997, 2002)own structural–dynamic models of ues discussed in Section 5.4.5,growthcannot for ecosystem organisation and thermodynamics. long exceed the weakest capacity. On the other Each of these approaches, even when applied hand, capacity in excess of the threshold sat- directly to phytoplankton ecology, has its inher- urates processing: it does not make organisms ent weaknesses and these have long been recog- grow faster. nised (Levins, 1966). The first type simulates an So, how can the growth rates of natural pop- indirect relationship with accuracy and some pre- ulations in the field be modelled? The approach cision but lacks general applicability. The sec- advocated by Reynolds and Irish (1997)wasto ond has a small number of variables and yields suppose that the photautotrophic plankter does accurate and often precise information but only not grow anywhere better than it does in the under very conditioned circumstances. The third contrived culture conditions in the laboratory. achieves accuracy and applicability through gen- Given that the best growth performances of erality, at the cost of all precision. given species occur under ideal culture condi- Modelling philosophy and (certainly) comput- tions, that they are consistent and that between- ing power has moved on. Several attempts to species differences in growth rate are systematic compound specific process models of the sec- (Reynolds, 1984b), an ‘upper base line’ for simu- ond type into more comprehensive growth sim- lating natural population growth could be pro- ulations have been rather unsuccessful, except posed (Reynolds, 1989b). Three equations were where one or other of the components contin- invoked to predict attainable growth rate in the 236 GROWTH AND REPLICATION OF PHYTOPLANKTON

field. In the best traditions of Eppley’s (1972) Thus, the solution to Eq. (5.9)incorporated in model of phytoplankton growth, two of the to the growth-rate model is: equations set the growth potential to water tem- −1 −1 r θ, d = [rθ (24 h ) ] · ln 2I · perature. The first equation (5.5)predicts repli- ( I ) m 0 ◦ −1 0.236 −1 −1 cation rate at a standard 20 Casafunction of 0.257(msv ) · rθ ε (5.13) algal morphology. The second equation (5.6)provides the information to adjust specific growth Equation (5.13)isthus the third of the three rate to other temperatures. These predictions are equations written into the model that eventu- applied to an inoculum (or, in reiterations) to the ally became known as PROTECH. It remained incremented standing crop to simulate day-on- under development and testing for several years, day accumulation. This has to be linked, through but this central core has remained intact. An aloopinthemodel logic, to an inventory of important adjustment in respect of dark respi- resource supply, which checks that a given daily ration was incorporated into the model that was increment is sustainable and, if so, to permit the eventually published (Reynolds et al., 2001). This growth step to be completed. A further feedback followed the important steps of sensitivity test- loop deducts the consumption from the pool of ing, authentication and validation (Elliott et al., available resources. 1999a, 2000a). It has been used to make realistic Insofar as the depth-integration of light inten- reconstructions of phytoplankton cycles of abun- sity and the duration of daylight impose, almost dance and composition (by functional type) in everywhere on the surface of the planet, a sub- lakes and reservoirs (Elliott et al., 2000a;Lewis ideal environment with respect to continuously et al., 2002). It has been applied to simulate light-saturated cultures, the sensitivity of species- succession in undisturbed environments (Elliott specific growth sensitivity to insolation is written et al., 2000b)andtoinvestigate the minimum into the third of the model equations. The orig- size of inoculum for the growth rate still to inal model supposed that the insolation-limited enable an alga to attain dominance (Elliott et al., specific growth rate is in proportion to the frac- 2001b). Vertical mixing can be used as a vari- tion of the day that the alga spends in the light: able to disturb community assembly (Elliott et al., 2001a)and to evaluate selective impacts of −1 = / r(θ,I )d rθ tp 24 (5.9) intearctions between variations in mixing depth and in surface irradiance (Elliott et al., 2002). PRO- where the daily sum of photoperiods, t , comes p TECH models exist with differing physical drivers from: (PROTECH-C, PROTECH-D), that work in coastal

tp = hp/hm (5.10) waters (PROTECH-M) and which are dedicated to (specific) rivers (RIVERPROTECH). Versions have where hm is the mixed depth and hp is the height been prepared for numerous UK and European of the light compensated water column, which, lakes and reservoirs, with accumulating success. following Talling (1957c;seealso Section 3.5.3)is At time of the writing, summary papers are still solved as: in press. = / . ε−1 hp ln(I0 0 5Ik) (5.11) where I 0 is the daily mean irradiance immedi- 5.6 Summary ately beneath the water surface (in µmol photon −2 −1 ε m s )and is the coefficient of exponential Cell replication and population growth are con- light attenuation with depth. The onset of light sidered as a unified process and accorded expo- limitation of growth, Ik is here related specifically nential logarithmic units with the dimensions of to the algaviaEq.(5.12): time. The observed rates of population change in ± = α−1 nature ( rn)are net of a series of in-situ rates of Ik rθ r (5.12) loss (rL,treated in Chapter 6). However, the true −1 0.236 where αr = 0.257 (msv ) (Eq. 5.8). ratesofreplication (r )mustalwaysbewithin SUMMARY 237

(and are sometimes well within) the least rate species having weaker affinities and may outper- that is physiologically sustainable on the basis of form them by building up larger inocula than theresources supplied. Cell replication is regu- potential competitors. Chronic or eventual defi- lated internally and cannot occur without the ciencies in nitrogen may have an analogous selec- prior mitotic division of the nucleus. Nuclear tive effect, although, subject to the fulfilment of division is prevented if the cell does not have other criteria (available phosphorus, high insol- the resources to complete the division. If it does, ation and a supply of relevant trace metals; replication can proceed at a species-specific max- see Chapter 4), dinitrogen fixers may experience imum rate. selective benefit. In general, division rates are strongly reg- In the frequent cases in which nutrient deple- ulated by temperature. Species-specific division tion is experienced first in the near-surface ◦ rates at 20 C(r20)arecorrelated with the surface- waters of the upper mixed layer and proceeds to-volume (sv−1)ratios of the algal units, as downwards, high affinity may be less help- are the slopes of the temperature sensitivity of ful than high mobility. The beneficial ability growth. The light sensitivity of growth is sub- to undertake controlled downward migration ject to physiological photoadaptation but, ulti- with respect to the relevant ‘nutricline’ or to mately, the shape of the alga influences its effec- perform diel or periodic forays through an tiveness as a light interceptor. Species which offer increasingly structured and resource-segregated ahigh surface-to-volume ratio through distortion medium, is conferred through the combination from the spherical form (such that the maxi- of self-regulated motility and large organismic mum linear dimension, m,israthergreaterin size. The greater is the isolation of the illumi- one plane than in one or two of the others) nated, nutrient-depleted, upper column from the and show high values of the product msv−1 are dark but relatively resource-rich lower column, indicative of probable tolerance of low average thegreater is the value of such performance- insolation. Given that the potential daily photon maintaining adaptations. harvest becomes severely constrained by vertical In the face of silicon shortages, diatoms mixing through variously turbid water to depths are unable to perform at all, whereas the per- beyond that reached by growth-saturating levels formances of non-diatoms is normally consid- of downwelling irradiance, enhanced light inter- ered insensitive to fluctuations in supply. The ception becomes vital to maintaining growth. amounts of silicon required vary interspecifi- Below a threshold of about 1–1.5 mol photons cally, as do the affinities for silicic-acid uptake. m−2 d−1,growth-rate performances are main- Because diatom nuclei divide before the silicic tained relatively better in plankters offering the acid needed to form the daughter frustules is combination of relevant morphological preadap- taken up, it is possible for otherwise resource- tation and physiologically mediated photoadap- replete and growing populations to experience tative pigmentation. big mortalities as a consequence of sudden Growth rates of phytoplankton species are var- encounter with Si limitation. With other nutri- iously sensitive to nutrient availability, though ents, planktic algae are able to ‘close down’ not at concentrations exceeding 10−6 MDIN vegetative growth and to adopt a physiologi- or 10−7 M MRP. Above these ‘critical’ levels, cal (or perhaps morphological) resting condition, growth rates are neither nitrogen nor phospho- which improves the survival prospects for the rus limited. Neither, it is argued, are they depen- genome. dent upon the ratio of either of these resources The environments of phytoplankton may be to the other.However,differing species-specific classified, following Grime (1979), upon their nutrient-uptake affinities influence the potential ability to sustain autotrophic growth, in terms growth performances when nutrient availabili- of the production that the resources will sus- ties fall to, or are chronically below, the ‘critical’ tain and the duration of the opportunity. Most levels. Species with high affinity for phosphorus algae will grow under favourable, resource- are able tomaintainafasterrateofgrowththan replete conditions during long photoperiods. The 238 GROWTH AND REPLICATION OF PHYTOPLANKTON

species that perform best rely on an early pres- resource-gathering constraints against large size ence, rapidity in the conversion of resources but the smallest picoplanktic sizes of photoau- to biomass and a high frequency of cell divi- totrophs have these provinces of the aquatic envi- sion and recruitment of subsequent generations. ronment very nearly to themselves. It is proposed By analogy with Grime’s (1979) functional clas- here that they be henceforth referred to as ‘SS sification of plants, these algae are considered strategists’. to be C strategists; they aretypically small Many algae have adaptations and biologies (<103 µm3), usually unicellular, have high sv−1 that represent intermediate blends of C-, S- or R- ratios (>0.3 µm−1) and sustain rapid growth strategist adaptations and lifestyles. The spatial −1 rates (r 20 > 0.9 d ). Algae whose growth per- and temporal distributions of particular types formance is relatively tolerant of and adaptable and species of phytoplankton, and the opportuni- to progressively shorter photoperiods and aggre- ties of replication that lead to population devel- gate light doses are comparable to Grime’s rud- opment, are shown to be closely correlated with eral (R)strategists: their sizes are varied (103–105 the extent of their C, S or R attributes. Though µm3)butall offer favourable msv−1 ratios (range best demonstrated among the freshwater phyto- 15–1000). Algae whose growth performances are plankton, the functional–strategic approach of maintained in the face of diminishing nutri- Grime appears to hold just as well for the ecolo- ent availability are equipped to combat resource gies of the marine plankton. In both the sea stress. Their conservative, self-regulating S strate- and fresh waters, morphological and (presum- gies are served by the properties of large size ably) physiological criteria are better predictors (104–107 µm3)andmotility but at the price of of ecology than are phylogenetic affinities. In a low sv−1 (<0.3 µm−1), low msv−1 (<30) and slow concluding section, this finding is reversed to −1 rates of growth (r 20 <0.7 d ). show how functional properties of phytoplank- Neither large size nor motility offer any tonand their respnses to environmental drivers advantage to survival in chronically resource- can be used to predict the structure of ascen- stressed environments of the ultraoligotrophic dent phytoplankton communities on the basis of oceans and the largest lakes. Moreover, the their likely strategic growth responses and not extreme resource rarification also offers a respite thestochasticity of the processes befalling indi- from direct consumption. Not only are there vidual species. Chapter 6

Mortality and loss processes in phytoplankton

wasalmost wholly and precisely compensated 6.1 Introduction by simultaneous bulk loss rates (Forsberg, 1985), when the rates of grazing or sedimentation This chapter considers the sinks and, more par- might only rarely explain the disappearance of ticularly, the dynamic rates of loss of formed theequivalent of the day’s new product, it cells from phytoplankton populations. Several became clear that some further separation of the processes are involved -- hydromechanical trans- ‘losses’ was necessary, together with some refine- port, passive settlement and destruction by her- ment of the terminology. Here, adjustments to bivores and parasites -- which, separately or in the photosynthate content that the cell is unable concert, may greatly influence the structuring to deploy in new growth or to store intracellu- of communities and the outcome of compet- larly and which must be dispersed through accel- itive interactions among phytoplankton. More- erated respiration, or photorespiration, or secre- over, these same processes may contribute power- tion as glycollate or other extracellular product, fully to the biogeochemical importance of pelagic are considered to be ‘physiological’. The adjust- communities, through their role in translocating ments are as much to protect the intracellular bioproducts from one point of the planet’s sur- homeostasis as to supply any other component of face to another. thepelagic system. On the other hand, success- Before expanding upon these processes, how- fully replicated cells in growing populations are ever, the opportunity is taken to emphasise that continuously but variably subject to physical or the losses considered in this chapter are those biological processes that deplete the pelagic con- that affect the dynamics of populations. The centrations in which they are produced. Detract- (sometimes very large) loss of photosynthate pro- ing from the numbers of new cells added to duced in excess of the cell’s ability to incorpo- the population, these losses are ‘demographic’ rate in biomass is not considered here. The topic and, as such, are the proper focus of the present is covered in a different context in Chapter 3 chapter. Its objective is to establish the quantita- (see especially Section 3.5.4). The emphasis is nec- tive basis for estimating the drain on the poten- essary as the term ‘loss rates’ was applied col- tial rate of recruitment, provided by cell repli- lectively to the dynamics of almost all measur- cation, that is represented by the counteracting able photosynthetic production that did not find processes which, effectively, dilute the recruit- its way into increased producer biomass (Jassby ment of phytoplankton biomass. In the sense of and Goldman, 1974a). It had been supposed by Eq. (5.3), the task is to quantify the magnitude many workers at the time that the realised short- and variability in the rates of dilution of finished fall was attributable to grazing and sedimenta- cells (rL). tion of biomass. However, with the demonstra- As already suggested, the principal loss pro- tion that, very often, production in some systems cesses are hydomechanical dispersion (wash-out 240 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

from lakes, downstream transport in rivers, patch theresidual population. The essential question is dilution at sea), sedimentation and consumption whether the inflow simply replaces the original by grazers. Attention is also accorded to mor- volume by direct displacement or by a flushing talities through parasitism (a specialised con- action, in which the inflow volume mixes exten- sumption) and physiological death and wastage. sively with the standing volume, displacing an Although highly disparate in their causes, each equivalent volume of well-mixed water. In the lat- process has the effect of diluting the locally ran- ter case, the original volume and the algal pop- domised survivors. Hence, each is describable ulation that it entrained will have been depleted by an exponent, summable with other loss and less completely and will now be, on average, less growth terms. Just as Eq. (5.1)explains the rate dilute. of population change, δN /δt,byreferenceto the first-order multiplier, ernt,andwhere,from 6.2.1 Expressing dilution Eq. (5.3), it may be asserted that rn = r − rL,it The mathematics of dilution are well estab- may now be proposed that: lished. Dilution of the standing volume and its suspended phytoplankton is described by r = r + r + r + r ... (6.1) L W S G an exponential-decay function. Until Uhlmann’s

where rW, rS, rG ... aretherespective exponents (1971) consideration of the topic, there had been for the instantaneous rates of biomass loss due few attempts to express the dilution of phyto- to wash-out, sedimentation, grazing, etc. It is plankton by displacement. He was quick to see accepted that these terms, either individually or and to exploit the opportunity to put losses in the in aggregate, may raise rL > r ,inwhich case, rn same terms as recruitment (cf. Eq. 5.3) and simply is negative and symptomatic of a declining pop- sum the instantaneous exponents. As depletion ulation. rates to settlement and some forms of grazing The following sections will consider the mag- succumb to analogous exponential functions, it nitudes and variabilities of the loss terms. is perhaps helpful to rehearse the logic that is invoked. In the present case of dilution by wash-out, 6.2 Wash-out and dilution we suppose that a population of uniform, non- living, isopycnic particles (N0)isfully entrained The hydraulic displacement and dispersion of and evenly dispersed through the body of a brim- phytoplankton is best approached by considering full impoundment of volume, V.The introduc- the case of algae in small lakes or tidal pools tion of a volume of particle-free water, qs,in in which the volume is vulnerable to episodes unit time t,displaces an equal volume into the of rapid flushing. Inflow is exchanged with the outflow from the impoundment. Thus, the the- instantaneous lake volume and embedded plank- oretical retention time of the impoundment, tr, tic cells are removed in the outflowing volume is given by V/qs. The outflow volume will carry that is displaced. In this instance, the algae thus some of the suspended particles. From the ini- removed from the water body are considered tial population (N0), particles willberemovedin ‘lost’. It may well be that the individuals thus the proportion −qs/V.Afteragivenshort time ‘lost’ will survive to establish populations else- step, t,the population remaining, Nt,iscalcula- where. Indeed, this is an essential process of ble from: species dispersal. The balance of the original pop- N = N (1 − q t/V ) (6.2) ulaton that remains is, of course, now smaller t 0 s and, occupying the similar volume of lake, on During a second time period, of identical length average, less concentrated. The predicted net rate to the first, an equal proportion of the original of change in the depleting population may be off- might be removed but only if the remainder orig- set or possibly compensated by the simultaneous inal population has not been intermixed with rate of cell replication but, for the moment, we and diluted by the inflowing water. If there is shall consider just the effects of biomass loss on mixing sufficient to render the residue uniform WASH-OUT AND DILUTION 241

at t,then, at t2,weshould have: critical factor in the population ecology of phytoplankton. At the mesoscales of patch formation, N = N (1 − q t/V ) 2 t s where recruitment by growth is pitched against = − / − / . N0(1 qs t V )(1 qs t V ) dilution through dispersion, it is possible to con- Thus, after i such periods of length t, sider V as the patch size and qs as the rateofits horizontal diffusion as being critical to the main- = − / i Ni N0(1 qs t V ) (6.3) tenance of patchiness (the models of Kierstead and Slobodkin, 1953;Joseph and Sendner, 1958; and after one lake retention time (tw) see also Section 2.7.2). In lakes much smaller = − / tw/t 2 Ntw N0(1 qs t V ) (6.4) than 10 km in area, wherein the maintenance of large-scale developmental patches is largely This is, of course, an exponential series, which untenable (that is, critical patch size usually quickly tends to exceeds the horizontal extent of the basin and = −1 Ntw N0 e (6.5) any small-scale patchiness is very rapidly averaged) the proportion of q to V assumes increas- where e is the natural logarithmic base. Equa- s ing importance. While t > 100 days, small dif- tion (6.5)hasadirectmathematical solution w ferences in hydraulic throughput may remain (N = 0.37N ) which predicts that, at the end tw 0 empirically inconsequential in relation to poten- of one theoretical retention time, the volume −1 tial growth rate: rw is <0.01 d .Its doubling to diluted by flushing retains 0.37 of the original − 0.02 d 1 is still small in relation to the rates of population. Had the same volume simply been growth that are possible. However, when the lat- displaced by the inflow, the retained population ter are themselves severely limited by environ- would have fallen to zero. These possibilities rep- mental conditions, dilution effects can become resent the boundaries of probable dilution, lying highly significant. In the instance of Planktothrix between complete mixing with, and complete dis- agardhii considered in Section 5.4.5,performing placement by, the inflow volume. at its best to grow under the mixed conditions Supposing the tendency is strongly towards of a temperate lake in winter, its replication rate the flushing of algae by inflow, Eq. (6.5)maybe − of 0.16 d 1 will be insufficient to counter out- used to estimate the residual population at any − wash losses when t ≤ 7days(r ≥−0.16 d 1). given point in time, t,solongasthe same rates w w If it is growing less well, the sensitivity to flush- of fluid exchange apply: ing clearly increases. Temperate lakes regularly −t/tw Nt = N0 e experiencing retention times less than about −qst/V 30 days seem not to support Planktothrix popu- = N0 e (6.6) lations. In the persistently spring-flushed Mon- To now derive a term for the rate of change tezuma’s Well, Arizona, studied by Boucher et al. in the standing population that is attributable (1984)(tw < 9 d), the distinctive phytoplankton to outwash (rw in Eq. 6.1)isquite straightfor- comprises only fast-growing nanoplanktic species. ward, provided that the time dimension of the In the English Lake District, some of the lakes − − inflow rate (s 1,d 1)iscompatible with the other have volumes that are small in relation to their terms. largely impermeable, thin-soiled mountainous catchments, and which episodically shed heavy rw = qs /V (6.7) rainfall run-off (1.5--2.5 m annually). In Grasmere (tw ∼ 24 d annual average but, instantaneously, 6.2.2 Dilution in the population ecology of rangingfrom5dto∞), Reynolds and Lund (1988) phytoplankton showed that the phytoplankton had almost to At first sight, the magnitude of hydraulic dis- recolonise the water column after wet weather, placement rates (qs)relative to the scale of stand- while it required a long dry summer for Anabaena ing volume in large lakes and seas seems suffi- to become established. Wet winters also keep ciently trivial for outwash to be discounted as a phytoplankton numbers low but, in the relatively 242 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

dry winter of 1973, the autumn maximum of physics of river flow and on the adaptations Asterionella persisted to merge with the spring and population dynamics of river plankton (pota- maximum. moplankton) developed quickly during the mid- 1980s. These were reviewed and synthesised by 6.2.3 Phytoplankton population dynamics Reynolds and Descy (1996)inanattemptto in rivers assemble a plausible theory that would explain The most highly flushed environments are rivers. theparadoxes about potamoplankton. The prin- Larger ones often do support an indigenous cipal deduction is that rivers are actually not phytoplankton, usually in at least third- or very good at discharging water. Not only is their fourth-order affluents, and sometimes in very velocity structure highly varied, laterally, verti- great abundance (perhaps an order of magni- cally and longitudinally, but significant volumes tude greater concentration than in many lakes; I (between 6% and 40%) may not be moving at all. have an unpublished record of over 600 µgchla Apartofthisnon-flowingwater is, depending L−1 measured in the River Guadiana at Mourão, on the size of the stream, explained in terms of Portugal, under conditions of late summer flow). boundary friction with banks and bed but a large The ability of open-ended systems, subject to per- part is immobilised in the so-called ‘fluvial dead- sistent unidirectional flow, to support plankton zones’ (Wallis et al., 1989; Carling, 1992). These is paradoxical. It is generally supposed to be a structures are sufficiently tangible to be sensed function of the ‘age’ of the habitat (length of the remotely, either by their differentiated tempera- river and the time of travel of water from source ture or chlorophyll content (Reynolds et al., 1991; to mouth), for there is no way back for organ- Reynolds, 1995b). They are delimited by shear isms embedded in the unidirectional flow. On the boundaries across which fluid is exchanged with other hand, the wax and wane of specific popula- the mainflow.Thespecies composition of such tions in given rivers seem fully reproducible; they plankton they may contain is hardly different are scarcely stochastic events. Moreover, some from that of the main flow but the concentra- detailed comparisons of the mean time of travel tion may be significntly greater. It has also been through plankton-bearing reaches of the River shown that the enhancement factor is a function Severn, UK, with the downstream population of the fluid exchange rate and the algal growth increment would imply rates of growth exceeding rate: the longer cells are retained, the greater is those of the best laboratory cultures (Reynolds the concentration that can be achieved by grow- and Glaister, 1993). Downstream increases in the ing species before they are exchanged with the phytoplankton of the Rhine, as reported byde flow (Reynolds et al., 1991). Each dead-zone has its Ruyter van Steveninck et al. (1992), would require own V and qs characteristics and its own dynam- specific growth performances paralleling any- ics. The analogy to a little pond, ‘buried in the thing that could be imitated in the laboratory. river’ (Reynolds, 1994b), is not entirely a trite one. It was also puzzling how the upstream inoc- Reynolds and Glaister (1993)proposed a model to ula might be maintained and not be themselves show how the serial effects of consecutive fluvial washed out of a plankton-free river (Reynolds, dead-zones contribute to the downstream recruit- 1988b). ment of phytoplankton. The recruitment is, nev- These problems have been raised on many pre- ertheless, sensitive to changes in discharge, fluid vious occasions and they have been subject to exchange and turbidity. It proposes a persistent some important investigations and critical anal- advantage to fast-growing r-selected opportunist yses (Eddy, 1931;Chandler, 1937;Welch,1952; (C-strategist) phytoplankton species or to process- Whitton, 1975). However, it was not until rel- constrained (CR-strategist) ruderals, as later con- atively more recently that the accepted tenets firmed by the categorisation of potamoplankters advanced by the classical studies of (such as) of Gosselain and Descy (2002). Zacharias (1898), Kofoid (1903)andButcher(1924) The model does not cover the many other could be verified or challenged. New, quantita- fates that may befall river plankton or influ- tive, dynamic approaches to the study of the ence its net dynamics, especially consumption SEDIMENTATION 243

by filter-feeding zooplankton and (significantly) not exceeding the quotient hw/ws (Section 2.6.2): zoobenthos, including large bivalves (Thorp and t = h /w s (6.8) Casper, 2002;Descyet al., 2003). Neither does it w s cover explicitly the issue of the perennation of The point that has been made at length and on algal inocula. However, in reviewing the avail- many previous occasions is that planktic algae able literary evidence, Reynolds and Descy (1996) do not inhabit a static medium but one that is argued for the importance of the effective mero- subject to significant physical movement. Forcing plankty to centric diatoms whose life cycles of its motion by buoyancy, tide, wind, Coriolis conspicuously include benthic resting stages effect is resisted by the viscosity of the water. This (Stephanodiscus and Aulacoseira,bothcommon in resistance is largely responsible for the charac- potamoplankton generally, have proven survival teristically turbulent motion that predominates ability in this respect). They also cited the remark- in surface waters of the sea, in lakes and rivers able studies of Stoyneva (1994) who demonstrated (see Section 2.3). Moreover, the turbulent veloci- the roleofmacrophytesasshelters and substrata ties so overwhelm the intrinsic velocities of phy- for many potamoplanktic chlorophyte species. toplankton sinking that the organisms are effec- The presence of such plants, in headwaters and tively entrained and randomised through tur- in lateral dead-zones, provides a constant source bulent layers. However, it may be emphasised of algae that can alternate between periphytic again that turbulent entrainment does not over- and planktic habitats. This is little different from come the tendency of heavy particles to sink rel- the proposition advanced by Butcher (1932)over ative to the adjacent medium and, in bound- 60 years before. His prognoses about the sources ary layers and at depths not pentrated by turbu- of potamoplankton remain the best explanation lence, particles are readily disentrained and more to theinoculum paradox and the one aspect still nearly conform to the behaviour expressed in awaiting quantitative verification. Eq. (2.16). Following Humphries and Imberger (1982), thecriterion for effective entrainment ( )isset 2 1/2 6.3 Sedimentation by Eq. (2.19) (i.e when ws < 15[(w ) ] )andis illustrated in Fig. 2.16. The depth of the mixed 6.3.1 Loss by sinking layer over which it applies (hm)may be calculated Most phytoplankters are normally heavier than from the Monin--Obukhov and Wedderburn for- the water in which they are dispersed and, there- mulations. It may often be recognisable from the − fore, tend to sink through the adjacent medium. vertical gradient of density (δρw ≥ 0.02 kg m 3 −1 The settling velocity (ws)ofasmallplanktic alga m ) (Section 2.6.5)or, casually, from inspection that satisfies the condition of laminar flow, with- of the vertical distribution of isotherms. out frictional drag (Re < 0.1), may be predicted by The estimation of sinking loss rates from a themodified Stokes equation (2.16;seeSections fully mixed water column (H)oramixedlayer 2.4.1, 2.4.2): (hm)applies logic analogous to the dilution by wash-out of a fully dispersed population of parti- 2 −1 −1 ws = g(ds ) (ρc − ρw)(18ηφr ) ms (2.16) cles subject to leakage across its lower boundary. Moreover, as sinking loss is the reciprocal of pro- where ds is the diameter of a sphere of identical longed suspension, it is relatively simple to adapt ρ − ρ volume to thealga, ( c w)isthedifference Eqs. (2.20--2.25)tothesequenceof steps traced in between its average density and that of the water, Eqs. (6.3--6.6)and to be able to assert that popula- φ and r is the coefficient of its form resistance tion remaining in the column, hm,attheendof owing to its non-sphericity; η is the viscosity of aperiod, t,ofsustainedand even sinking losses the water, and g is the gravitational force attrac- is predicted by: tion. In completely still water, particles may be = −t/t expected to settle completely through a column Nt N0 e −ws t/hm of water of height hw within a period of time (t ) = N0 e (6.9) 244 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

− ws = 0.3m d 1 Figure 6.1 Biomass-speciﬁc − ws = 1.0m d 1 sinking loss rates of phytoplankters from mixed columns as a function of w = 3.0m d−1 − 1 s their depth and intrinsic settling rates (w s). Three instances are inserted to show the greater rate / d rate / tolerance of shallow mixing by slow-sinking algae. Redrawn with permission from Reynolds (1997a).

depth / m

Whence, the rate of change in the standing taining net intracellular carbon accumulation population that is attributable to sedimentation and its deployment in growth are increased (rs in Eq. 6.1)is: accordingly (Section 3.3.3;seealso Sverdrup, 1953;Smetacekand Passow, 1990;Huisman = / rs ws hm (6.10) et al., 1999). It must be recognised that, in qual- The equation expresses the sinking loss rate sus- itative terms, larger non-motile plankters expe- tained by a population dispersed in a mixed rience mixing that is ‘too shallow’ for growth to layer. overcome their sinking velocity (because hm is rel- It may be deduced that the continued resi- atively small in relation to ws in Eq. 6.10)oris‘too dence of non-motile particles in the pelagic is deep’ (because hm is relatively much larger than dependent not only on having maximum entrain- hp in Eq. 5.10;see also Section 3.5.3 and Fig. 3.18) (O’Brien et al., 2003; see also Huisman et al., ability (low ws)butalso on the settling velocity 2002). being small in relation to the mixed depth, hm.As discussed in Section 2.6,thedepthofmixingis an extremely variable quantity. Disentrainment 6.3.2 Mixed depth and the population is not a disadvantage for a swimming organism, dynamics of diatoms especially not a large one, but non-motile organ- Included among the larger non-motile plankters isms are highly vulnerable to variations in mixed are some of the larger freshwater desmids and, depth (see Fig. 6.1). The growth rate of an alga especially, the diatoms of the seas and of inland with an intrinsic sinking rate of 3.5 µms−1 (or waters. The additional ballast that is represented ∼0.3 m d−1)maybeableto exceed the leak- by the complement of skeletal polymerised silica age of sinking cells across the base of a 10-m merely compounds the density difference compo- −1 mixed layer (rs ∼−0.03 d )but,injust2m nent, (ρc − ρw), in Eq. (2.16). Accepting that most −1 (rs ∼−0.15 d ), the sinking loss rate may become species of phytoplankton are required to be either unsustainable. Species with greater settling rates small or motile or to minimise excess density if experience proportionately more severe loss rates they are to counter the inevitability of mixed- from any given mixed layer. Thus, they require layer sinking losses, it is striking how poorly the yet deeper mixed layers to sustain positive diatoms represent all three attributes. Yet more net growth. On the other hand, greater mix- perplexing is the fact that the planktic diatoms ing depths quickly begin to impose constraints of freshwaters are relatively more siliciﬁed that of inadequate photoperiod-aggregation (see Sec- their marine cousins (effectively raising ρc; Sec- tions 5.4.1, 5.5.3), and the difﬁculties of sus- tion 1.5.2 and Fig. 1.9), while the density of many SEDIMENTATION 245

non-saline inland waters (ρw)islessthanthat theseasonal variations in the vertical distribu- of the sea. Thus, the density difference of some tion of Asterionella formosa in the North Basin freshwater diatoms may exceed 100−200 kg m−3 of Windermere (Fig. 2.21). The build-up in num- (cf. Table 2.3). How are we to explain how this bers during the month of April and, especially, group of organisms, so relatively young in evolu- towards the maximum in May reflect the general tionary terms, became so conspicuously success- decline in vertical diffusivity. In the end, a near- ful as a component of the phytoplankton of both surface concentration maximum is reached, fol- marine and fresh waters, when it has not only lowed by a rapid decline. In this instance, recruit- failed to comply to Stokes’ rules but has actually ment through growth was impaired by nutrient gone against them by placing protoplasts inside deficiencies (Lund et al. cited critical silicon lev- anon-living box of polymerised silica? There els but phosphorus is now seen likely to have is no simple or direct answer to this question, been the more decisive; see Section 5.5.2). How- although, as has been recognised, sinking does ever, it is quite clear from the isopleths that have positive benefits, provided that subsequent thedecline in concentration in the upper 10 generations experience frequent opportunities morsoisextremelyrapid.Itiscompensated, to be reintroduced into the upper water col- to an extent, by a temporary accumulation in umn (Section 2.5). In general, however, many of theregion of the developing pycnocline. This the ecological advantages of a siliceous exoskele- behaviour is entirely consistent with elimination ton wereexperienced first among non-planktic through sedimentation from the mixed layer and diatoms. As the diatoms radiated into the plank- slow settlement through the weak diffusivity of ton, morphologies had to adapt rapidly: siliceous themetalimnion, revealed in the case of non- structures mutated into devices for enhancing living Lycopodium spores (Fig. 2.20). Particles conform resistance and entrainability within turbu- tinue to settle through the subsurface layers for lent eddies (Section 2.6). As was demonstrated many weeks after the population maximum and, in the case of Asterionella in the experiments indeed, after the surface layer has become effec- of Jaworski et al. (1988)(seealsoSection 2.5.3), tively devoid of cells. the configuration of the structures is overriding. Heavy sinking losses are not exclusive to Despite order-of-magnitude variations in colony nutrient-limited diatom populations. The sensi- volume and dry mass, aswellasanapproxi- tivity of the population dynamics of diatoms to mate twofold variation in cell density, the sink- the onset and stability of thermal stratification in ing behaviour of Asterionella remains under the Crose Mere, a small, enriched lake in the English predominating influence of colony morphology. north-west Midlands, rather than to nutrient lim- The corollary must be that the advantage of itation, was shown by Reynolds (1973a). Diatoms increased form resistance, and its benefits to such as Asterionella, Stephanodiscus and Fragilaria entrainability, is greater than the disadvantage of were lost from suspension soon after the lake increased sinking speed incumbent upon coeno- stratified in late spring, even though the con- bial formation. The counter constraint, however, centrations of dissolved silicon and phosphorus is that these diatoms are continuously dependent remained at growth-saturating levels. Lund (1966) upon turbulence to disperse and to randomise had already argued for the positive role of tur- them within the structure of the surface-mixed bulent mixing in the temporal periodicity of layer. As predicted by Eq. (6.10), positive popula- Aulacoseira populations. He showed, in a field- tion recruitment is always likely to be sensitive to enclosure experiment in Blelham Tarn (inciden- the absolute mixed-layer depth (Reynolds, 1983a; tally, the one that inspired the construction of Reynolds et al., 1983b;Huisman and Sommeijer, therenowned tubular enclosures in the same 2002). lake) that the periodicity could be altered readily The impact of this interplay between settle- by superimposing episodes of mechanical mixing ment and population dynamics of diatoms on by aeration (Lund, 1971). their distribution in space and time is elegantly Alittle later, the eventual Blelham enclosures expressed in the study of Lund et al. (1963)of (Fig. 5.11)were the site of numerous quantitative 246 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.2 Instances in the loss from suspension of Asterionella cells in Blelham Enclosure A during 1980, in response to intensifying thermal stratiﬁcation (shown by the temperature plots). Algal concentration is sampled in 1-m integrating sampler (Irish, 1980) and counted as an average for a 1- or 2-m depth band. The vertical arrows represent the depth of Secchi-disk extinction on each occasion. Redrawn from Reynolds (1984a).

studies of the fate of phytoplankton popula- md−1 (equivalent to 11.8 µms−1). The data are tions. One early illustration, cited in Reynolds plotted in Fig. 6.3. (1984a), shows the depletion by settlement of The accelerated sinking loss was contributed, athitherto-active Asterionella population, follow- in part, by an accelerated sinking rate. This was ing the onset of warm, sunny weather and the not unexpected. Reynolds and Wiseman (1982) induction of a stable, near-surface stratification, had noted the altered physiological condition and despite the availability of inorganic nutri- of the cells at the time, both in the plankton ents added to the enclosure each week (Fig. 6.2). and in the sediment traps, drawing attention In a further season-long comparison of loss pro- to the contracted plastids and ‘oily’ appearance cesses in these enclosures (Reynolds et al., 1982a), of the contents. They attributed the changes to during which changes in extant numbers, ver- thesudden increase in insolation of cells caught tical distribution, growth (as a function of sili- in a stagnating and clarifying (cf. Fig. 6.2)epil- con uptake) and sedimentary accumulation rates imnion at the same time that temperature and into sediment traps and at the enclosure bot- light intensity were increasing. They suggested tom wereallindependently monitored, a steady that the changes were symptomatic of photoin- ‘leakage’ of Asterionella cells was demonstrated hibition. When Neale et al. (1991b) made simi- over the entire cycle of net growth and attri- lar observations on diatom populations in other tion (see Table 5.5 and Reynolds and Wiseman, lakes, they made the similar deduction. A positive 1982). In the Blelham Enclosure B, Asterionella feedback implied by the sequence of more insola- − increased at a rate of 0.147 d 1 during its main tion → more stratification → more inhibition → phase of growth, net of sinking losses calcu- faster sinking rates → faster sinking loss rates has − lated tohavebeen∼0.007 d 1. The sedimenting asatisfying ring of truth. However, a modified cells intercepted by the traps were calculated to interpretation would see the accelerated sinking have been sinking at an average rate of (ws = ) rate as a withdrawal of the vital mechanism of − − 0.08 m d 1 (just under 1 µms 1)through a water reducing sinking rate (see Section 2.5.4)forthe column (hm = )11.7m.Asthepopulation reached very positive purpose of escaping the high levels its maximum, the net rate of increase slowed of near-surface insolation. − (to 0.065 d 1)butthesinking loss rate remained The bulk ‘production-and-loss budgets’ com- − steady (−0.007 d 1). However, shortening of the piled by Reynolds et al. (1982a)forphytoplank- mixing depth led to an accelerated rate of sink- tonpopulations in the Blelham Enclosures and − ing loss(to−0.044 d 1;fromamixeddepthof exemplified in Table 5.6 offer a clear account of now only 7.5 m, a faster sinking rate of ws = 0.33 thethe fate of the total production. In the exam- − md 1 is also implied). More remarkably, as the ple given, 81% (confidence interval, 70--95%) of epilimnion shrank to 4 m, the loss rate then rose the Asterionella formosa produced in Enclosure B − to −0.242 d 1,sustained by a sinking rate of 1.02 in the spring of 1978 constituted the observed SEDIMENTATION 247

recently recruited material) was 92% at the beginning of April. By the end of the month, it had fallen to 67%, to <2% by the end of July and to zero by the first week in September. As part of the same investigation, Reynolds and Wiseman (1982) compared the rates of production, sedimentary fluxes and sediment recruitment of several other species forming major populations in the same enclosures. Of theestimated summer production of another diatom, Fragilaria crotonensis,atleast 49% (statistically, possibly all) of the production was recruited to the sediments. In contrast, sedimentation could explain the fate of no more than 4% of the observed population maxima of Ankyra, Chromulina or Cryptomonas.Intermediate between the extremes of heavy diatoms and nanoplanktic unicells, sediment and trap recoveries of Eudo- rina accounted for 55 ± 15%ofthe maximum standing crops. For Microcystis,the sedimentary behaviour was strongly seasonal, increasing from 8% to 100% through the autumn. From the measurements of the production and eventual fate of phytoplankton in confined, Figure 6.3 Net increase and attrition of an Asterionella flat-bottomed Blelham enclosures, at least, the population cells in Blelham Enclosure B during spring 1978. (a) Changes in the instantaneous areal cell concentrations in assertion that most of the larger diatoms are the water to 3, 5 and 11 m; (b) changes in the silicon-specific destined to be lost to sedimentation is strongly replication rate (r Si) and the net rate of population change supportable. Scaling up to larger and deeper sys- (rn); the hatched areas correspond to the rate of population tems, subject to significant horizontal diffusive loss, almost wholly to sinking. Redrawn with permission from transport, the deduction requires some caution. Reynolds (1997a). In a 2-year study of sedimentary fluxes in the South Basin of Windermere (maximum depth 42 m), Reynolds et al. (1982b)found good, order-of- maximum. Around 95% (confidence interval, 72- magnitude agreement between the annual fluxes -123%) of the production was recruited intact to into deep sediment traps and the maximal stand- the sediment. The proportion of the cells pro- ing crops of five species of planktic diatom (Asteri- duced that was estimated to have been lost to onella formosa, Aulacoseira subarctica, Cyclotella herbivores was probably <6% (see Sections 6.4.2, praetermissa, Fragilaria crotonensis, Tabellaria floccu- 6.7). The use of the adjective ‘intact’ is taken losa var. asterionelloides)and two of desmid (Cosmar- to include cells that may well have been dead ium abbreviatum, Staurastrum cf. cingulum). Inter- by the timetheyreachedthesediment surface. estingly, the magnitude of the fluxes (in num- Judged from weekly recoveries from sediment bers of cells m−2 d−1)varied with the size of traps placed about ∼1mabovethesediment extant poulations but measurable fluxes to depth (and to which preservative was added), Reynolds persisted through most of the year. This is pre- and Wiseman (1982)observed that the propor- sumed to reflect the relative proportion of the tion of live cells was always greater than 89% particle settling rates to the vertical distance to throughout the course of the population rise and be traversed; this also fits with the observations decline. The proportion of live cells in the superfi- of Lund et al. (1963)fortheNorth Basin and the cial sediment (supposedly dominated by the most distribution of population isopleths plotted in 248 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Fig. 2.21.Incidentally, the proportion of live Aste- netic diatoms are subject. In most other phyto- rionella cells trapped fell from around 95% at the plankton, greater proportions are either eaten time of the May population maximum to just 3% or decompose long before they reach the sedi- in August and September. In the 100-or-so days ment. The deduction concurs with the studies of that it takes some diatoms to settle through 40 losses made by Crumpton and Wetzel (1982) and m, many must perish, leaving only the empty with that of Hillbricht-Ilkowska et al. (1979)in frustules to continue downwards. Jezioro Mikolajske, Poland, on the seaonal vari- In contrast to the diatoms, the sedi- ations in the main sinks of limnetic primary mentary fluxes of three colonial chlorophyte products. species (Coenochloris fotti, Pseudosphaerocystis lacus- The sensitivity of marine diatom dynamics tris, Radiococcus planctonicus), three Cyanobacte- to mixed-layer depth is not so clearly defined. ria (Anabaena flos-aquae, Woronichinia naegeliana, On the one hand, net population increase is Pseudanabaena limnetica)and the dinoflagellate dependent upon an enhancement in insolation Ceratium hirundinella were 1--3 orders of magni- above thresholds which may be lower than for tude smaller than the potential of the maximum many other marine species (Smetacek and Pas- standing crop. All these species either sink very sow, 1990) but the diminution of the mixed layer slowly or they have sufficient motility to avoid in the sea to the 1--3 m that may be critical to net being sedimented for long periods. Cryptomon- diatom increase is inconclusively documented. ads and nanoplankters were virtually unrecorded Nevertheless, oceanic diatom populations expe- in any trap catches; they are presumed to rience considerable sinking losses that may be have been subject to loss processes other than sustained only at or above certain levels of pro- settlement. ductivity. It is inferred that these are dependent These various findings supported the earlier upon adequate physical and chemical support deductions of Knoechel and Kalff (1978), who had (Legendre and LeFèvre, 1989;Legendre and applied a dynamic model to compare the effects Rassoulzadegan, 1996;seealso Karl et al., 2002). of measured rates of growth, increase and set- As to the question posed by Huisman et al. tlement in order to calculate sinking loss rates (2002)about the long-term persistence of sink- of planktic populations in Lac Hertel, Canada. ing phytoplankton, we have shown that there Their calculations showed that the rates of sink- are obvious short-term benefits in being able ing loss were sufficient to explain most of the dis- to escape surface stagnation and resultant dam- crepancy between growth and the contemporane- aging levels of insolation in the near-surface ous rate of population change, be it up or down. waters (Reynolds et al., 1986). Provided there is They were also able to provide quantified sup- an opportunity for surviving propagules to be report for the idea that, whatever fate may befall established within the photosynthetic range, the them (nutrient, especially silicon, exhaustion, sooner may the longer-term benefit of population grazing, parasitism), planktic diatoms remain re-establishment be realised. Particle aggregation crucially sensitive to the intensity and extent and, especially, the formation of ‘marine snow’ of vertical mixing. Other workers who espoused (Alldredge and Silver, 1988)maycontribute effec- this explanation for the seasonal fluctuations in tively to accelerated sinking and to the escape diatom development and abundance in limno- from high-insolated surface layers. Aggregation plankton include Lewis (1978a, 1986), Viner may also serve to provide microenvironments and Kemp (1983), Ashton (1985)andSommer that slow down the rate of respirational con- (1988a). sumption and resist frustular dissolution of sil- There is now also ample evidence to sup- icon (Passow et al., 2003). The mechanisms of port the qualitative contention of Knoechel and accelerated sinking may also add to the longevity Kalff (1975)that sedimentation is a key trig- of clone survival and facilitate the improved ger to the seasonal replacement of dominant prospect of population re-establishment when diatoms by other algae. It is also plain that sed- more suitable growth conditions are encoun- imentation is the principal loss to which lim- tered. SEDIMENTATION 249

6.3.3 Accumulation and resuspension of ticulate organic matter, the exuviae and exc- deposited material reta of aquatic animals and a rain of sedi- As has already been discussed, settling is not menting phytoplankters, especially of non-motile exclusively a loss process in the population diatoms. dynamics of phytoplankton: the recruitment of Several studies have attempted to focus on resting propagules to the bottom deposits is thenature of the freshly sedimented material recognised to constitute a ‘seed bank’ from which in lakes and its immediate fates. For a time, later extant populations of phytoplankters may thenewest recruited material remains substan- arise (see Section 5.4.6). For this to beaneffec- tially uncompacted and floccular, like a fluff, on tive means of stock perennation and mid- to theimmediate surface. It comprises live or mori- long-term persistence in a given system, how- bund vegetative cells, often bacterised or beset ever, there has to be a finite probability of set- with saprophytic fungal hyphae, and resembles tled material both surviving on the sediments on a smaller scale, the structure of ‘marine snow’ and, thence, of re-entering the plankton. The (Alldredge and Silver, 1988;seeSection 6.3.2). species-specific regenerative strategies of phyto- As its substance diminishes, however, it does plankton -- roughly their ability to survive at become slowly compressed by later-arriving mate- the bottom of the water column and the means rial. At the base of the semifluid layer, the same of ‘escape’ to the overlying water column -- are materials are progressively lost to the permanent extremely varied, ranging from the conspicuous sediment (Guinasso and Schink, 1975): compact- production of morphological and/or physiologi- ing, losing water, perhaps leaching biominerals, cal resting stages, with an independent capac- thefirst stages of sediment diagenesis and forma- ity for germination, regrowth and reinfection of tion are engaged. the water column (as in the case of Microcystis Accordingly, the manner in which strictly or Ceratium), through a range of resting cysts ordered, laminated sediments might flow from and stages whose re-establishment in the water the sequenced deposition of specific phytoplank- depends upon still-suspended or resuspended ton populations seems obvious. However, direct propagules encountering tolerable environmen- sampling of the semifluid layer from intact cores tal conditions (as is true for akinetes of nosto- of the sediment water interface (Reynolds and calean Cyanobacteria, certain species of volvo- Wiseman, 1982, used a syringe inserted into pre- calean and chrysophyte resting cysts and the dis- drilled plastic tubes fitted to a Jenkin surface- tinctive resting stages of centric diatom), to those mud sampler, as described in Ohnstad and Jones, that seem to make virtually no such provision at 1982)revealsthat sedimenting material under- all (see Section 5.4.6). goes a kind of sorting process. Once recruitment In most instances, the settlement of vege- to thesemifluid layer from the water column is tative crops should be regarded as terminal. effectively complete, its presence in the semifluid Vegetative cells sinking onto deep, uninsolated layer is found to decay exponentially. Moreover, sediments have little prospect but to slowly therates of dilution from the semifluid layer respire away their labile carbohydrates, pend- are not uniform but vary interspecifically, according depth. Resting cysts may remain viable for ing to size and shape (Haworth, 1976;Reynolds, many years (64 a is a well-authenticated claim 1996b): long cells of Asterionella,filaments of of viability of Anabaena akinetes: Livingstone Aulacoseira and chains of Fragilaria are diluted less and Jaworski, 1980)but without the mechanical rapidly from the semifluid layer than centric uni- resuspension of the resting spores in insolated, cells of Cyclotella or Stephanodiscus. nutrient-replete water, the reinfective potential Relative persistence in the surface layer remains unrealised. Once settled to the bottom improves the prospect of live specimens being of a water column, the most likely prospect is restored to suspension in the water column, sup- progressive burial by the subsequent sedimen- posing that the physical penetration of adequate tary recruitment of further particulate material, resuspending energy obtains. In general, friction including fine, catchment-derived silts and par- in the region of the solid sediments creates a 250 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

velocity gradient and a boundary layer of reduced greater than 5 m, sedimenting material accumu- watervelocities, in which freshly settled plank- lates and builds up in layers, undergoing dia- ton can accumulate (see Section 2.7.1). Resuspen- genesis under substantially anoxic conditions. sion is thus dependent upon the application of Neither live vegetative cells nor most resting sufficient turbulent shear force to compress the spores enjoy much prospect of return to suspen- boundary layer to the dimensions of the set- sion and regeneration. In contrast, similar mate- tled particles or even beyond the resistance of rials settling onto shallow sediments are liable the unconsolidated sediment to penetration by a to resuspension. The viable fractions (vegetative shear force, by then competent to entrain and cells, resting spores) may well fulfil their infec- resuspend it (Nixon, 1988). Quantitative obser- tive potential and contribute directly to the estab- vations confirm the intuition that shallow sed- lishment of extant, vegetative populations. This iments are rather more liable to resuspension has been many times observed in the case of than sediments beneath a substantial column of Aulacoseira populations (Lund, 1954, 1966, 1971) water, although the actual depth limits vary with and is inferred on other occasions involving sediment type and the energy of forcing (Hilton, other species (Carrick et al., 1993;Reynolds et al., 1985). In many small lakes, sediments at a depth 1993a). For the non-viable detritus, including greaterthan5mbeneaththewatersurfaceare empty diatom frustules, redeposition is the most protected from wave action and from most wind- likely consequence but with a finite proportion generated shear. In the short to mid term, resus- settling into deeper water. This is precisely the pension may require physical forcing of seismic mechanism of the process of ‘sediment focusing’ proportions, or depend upon disturbance by bur- (Lehman, 1975) whereby fine particulate material rowing invertebrates or foraging behaviour of is moved progressively away from lake margins fish or diving animal (Davis, 1974;Petr,1977). In and towards greater basin depths (Hutchinson, contrast, shallow sediments (substantially <5m) 1941;Likensand Davis, 1975;Hilton,1985) may be rather more routinely exposed to resuspension of sediment and, incidentally, the redispersion of sediment interstitial water that may 6.4 Consumption by herbivores be relatively enriched, with respect to the open water, with nutrients released in decomposition Sharing an apparently refugeless, open-water (see also Section 8.3.4). In the Blelham enclo- habitat with a variety of phagotrophic animals, sures (see Fig. 5.11), very little resuspension of phytoplankton is generally vulnerable to severe live phytoplankton, resting spores or even empty physical biomass losses and, at best, to the diatom frustules was observed from the universal dynamic drain on the potential recruitment deep sediments of Enclosures A or B but it was of biomass. In fact, there are many types of observed on numerous occasions in the graded consumer, each with differing food preferences Enclosure C (Reynolds, 1996b). Moreover, distur- and habitat demands, making for an extremely bance or removal of the semifluid sediment from wide range of possible outcomes. The subject of the shallow-water station, CS (Fig. 5.11,depth food and feeding is, indeed, a broad one, and ∼4.5 m), occurred at such times, whereas, the rather beyond the remit of the present chapter, deeper station, CD (depth ∼12.5 m) was exempt thefocus of which will remain trained on the from this. In the wake of such resuspension dynamic consequences for the producers. How- events, material was perceived to resettle uni- ever, even this modest ambition must take some formly at both stations. Over a series of resus- account of the biologies of the consumers and pensions, a net transport of once-settled material how their impacts fluctuate in time and space. from shallow areas to deep sites was deduced. What follows here is necessarily selective, So far as the accumulation of sediment- emphasising those aspects of zooplanktic biol- ing phytoplankton is concerned, near-permanent ogy which relate to phytoplankton dynamics and deposition follows analogous patterns to non- to the shaping of pelagic ecosystems. Numerous living particulate matter. At depths typically books and monographs describing the biology CONSUMPTION BY HERBIVORES 251 and ecology of particular zooplankton groups approach in preference to a taxonomic one. are available. Of the more general accounts, There are important differences in the composi- none had equalled those of Hutchinson (1967)or tion, ecological function and key selective mech- Raymont (1983), until the recent publication of anisms between the nano-/micro-planktic and Gliwicz’s (2003a)superboverview, to which the meso-/macro-planktic components and, indeed, reader is happily referred. The emphasis here among the principal types of mesozooplanktic is on crustacean herbivory, with only acknowl- association. edgement of the part played by small herbivorous fish in cropping phytoplankton in (usu- Protistan microzooplankton ally) small tropical lakes (see Fernando, 1980; In terms of numbers, the most abundant and Dumont, 1992). The present account also recog- most common zooplankters, both in lakes and nises that planktic primary products are con- in the sea, belong to the category of nano-/ sumed not only as the particulate foods of her- microzooplankton. This includes all planktic het- bivores but also as the dissolved substrates of erotrophs in the size range 2--200 µm, with aquatic microorganisms. theexception of the bacteria, actinomycetes and moulds (Sorokin, 1999). Rather than be pedan- 6.4.1 The diversity of pelagic phagotrophs tic about the nano--micro separation, it is con- and their foods venient to follow Sorokin’s (1999) usage of the Zooplankton comprises small animals suspended word ‘microzooplankton’ to apply to all het- in the water. Some (nanozooplankton and micro- erotrophic protistans and metazoans smaller zooplankton, all <200 µm) are truly planktic than 200 µm. This then includes representatives in the sense of being fully embedded in the of protistan groups already listed as phytoplank- eddy spectrum (Section 2.3.4)buteven most ton inTable 1.1 (especially Chrysophyta and Dino- larger forms of mesoplankton (0.2--2 mm) are phyta). As pointed out in Section 1.3,manyof toosmall and too weak to escape entrainment these are photoautotrophs with a phagotrophic by open-water currents. A characteristic of all capability (that is, that they are mixotrophic) but zooplankters is that they are partly or wholly themesoplanktic, colourless marine dinoflag- phagotrophic -- much or all of their organic ellates, such as Noctiluca and Oxyrrhis,are carbon and energy requirements are satisfied obligate phagotrophic consumers, feeding on by feeding onliveordetritalorganicparti- nanoplankters, including the haptophyte Prym- cles. Another feature of zooplankton, which, nesium (Tillmann, 2003). Freshwater mixotrophs broadly, is shared with phytoplankton, is the in the nanoplanktic size range include Chromu- cosmopolitan distribution of many genera and lina, Chrysococcus and Ochromonas. Chrysochromu- even some species. This may seem obvious in lina spp. and Prymnesium spp. fulfil this role in contiguous seas but it applies no less to the thesea (Riemann et al., 1995). They ingest par- plankton of inland waters. The main difference ticles in the picoplanktic size range, including between the zooplankton of seas and lakes is bacteria and algae. The nanoheterotrophs also the muchpoorer phylogenetic representation in include numerous small flagellated protists, clas- the latter. Whereas certain life-history stages of sified in Table 6.1 as Zoomastigophora. These certain species from almost every animal phy- have well-developed cytostomes and they are able lum occur in the marine plankton, limnoplank- to ingest substantial food particles, up to about ton mainly comprises protists, rotifers and crus- 5--8 µminsize. Free-living bodonids and pro- taceans. Major groups and representative plank- tomonadids are represented in the nanoplanktic genera are summarised in Table 6.1. tonoflakes and seas, where they can be effec- In briefly surveying the diversity of zooplank- tive consumers of nanophytoplankton. The group tonwithin the context of its quantitative impacts includes the choanoflagellates and bicosoecids on the phytoplankton and the flow of carbon that are usually attached to the surfaces of larger through the pelagic towards its larger metazoan plankters such as diatoms. At this scale, deep beneficiaries, it is useful to adopt a functional within the viscous range of the eddy spectrum 252 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Ta b l e 6.1 Zooplankton in marine and freshwater habitats

Phylum: Zoomastigophora Four orders of free-living and epiphytic or epizoic flagellates. Includes: Bodo, Monas, Peranema (marine and freshwater); Bicosoeca, Salpingooeca and Monosiga Phylum: Dinophyta Several families of marine dinoflagellate are mixotrophic or primarily heterotrophic. Includes: Dinophysis, Noctiluca, Oxyrrhis, Protoperidinium Phylum: Rhizopoda (Sarcodina) Four main divisions. Order: AMOEBINA Naked, lobose protists. Plantic genera include: Asterocaelum, Pelomyxa (freshwater) Order: FORAMINIFERA Amoeboid protists with non-calcareous shells. Includes: Globigerina (marine); Arcella, Difflugia (freshwater) Order: RADIOLARIA Marine planktic sarcodine protists having central capsule and usually a skeleton of siliceous spicules. Includes: Acanthometra Order: HELIOZOA Mostly freshwater sarcodines with axopodia and, typically, vacuolated cytoplasm and a siliceous skeleton. Includes: Actinophrys Phylum: Ciliophora Class: CILIATA Non-amoeboid protists that possess cilia during part of their life cycle: several planktic orders, including:

Order: HOLOTRICHA Uniformly ciliated. Includes: Colpoda, Prorodon, Pleuronema and freshwater Nassula Order: SPIROTRICHA Ciliates posessing gullet and undulating membrane. Includes many common genera of marine and freshwaters: Euplotes, Halteria, Metopus, Strobilidium, Strombidium, Stentor, Tintinnidium Order: PERITRICHA Ciliates, usually attached to surfaces. Cilia reduced over body and conﬁned to oral region. Includes: Epistylis, Vorticella, Carchesium Class: SUCTORIA Ciliophorans lose cilia in adult stage. Possess one or more suctorial tentacles. Includes: Acineta Phylum: Porifera Amphiblastula larvae temporally in marine plankton. CONSUMPTION BY HERBIVORES 253

Ta b l e 6.1 (cont.)

Phylum: Coelenterata Subphylum: Cnidaria Coelenterates with stinging nematocysts. Several orders have genera that live, or appear, in (mostly marine) plankton Class: HYDROZOA Order: LEPTOMEDUSAE Hydrozoan coelenterates with horny perisarc. Medusa stage in plankton. Includes: Obelia, Plumularia Order: ANTHOMEDUSAE Hydrozoan coelenterates with horny perisarc that does not cover polyp base. Medusa stage in plankton. Includes: Hydractinia Order: HYDRIDA Hydrozoan coelenterates without a medusa. Includes: Hydra,young hydroids of which disperse through freshwater plankton Order: TRACHYLINA Hydrozoan coelenterates with a relatively large medusa and minute hydroid stage. Includes: freshwater Limnocnida, Craspedacusta Order: SIPHONOPHORA Large, free-moving colonial hydrozoans. Includes: Velella, Physalia Class: SCYPHOZOA Cnidaria that exist mostly as medusae. Several orders. Includes: Aurelia, Cyanea, Pelagia Subphylum: Ctenophora Swimming coelenterates lacking nematocysts Class: TENTACULATA Ctenophores with tentacles (‘sea gooseberries’). Includes: Pleurobrachia Class: NUDA Ctenophores lacking tentacles. Includes: Bero¨e Phylum: Platyhelminthes Acoelomate metazoans (ﬂatworms, many parasitic) with a few free-living representatives in the marine plankton. Class: TURBELLARIA Includes: Convoluta, Microstomum Phylum: Nemertea Flattened unsegmented worms with a ciliated ectoderm and eversible proboscis. Several orders, one with planktic genera. Order: HOPLONEMERTINI Pilidium larvae of several genera are dispersed as marine plankton. Some genera remain bathypelagic, beyond the continental shelf, in their adult stages. Includes: Pelagonemertes 254 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Ta b l e 6.1 (cont.)

Phylum: Nematoda Unsegmented round worms. Some shelf-water species have been reported but these may not be truly planktic. Phylum: Rotatoria Acoelomate metazoans with planktic genera widespread in the sea and in lakes. Most planktic forms belong to one order, mainly in fresh waters. Order: MONOGONONTA Sub-order: Flosculariacea Free-swimming, soft-bodied. Includes: Conochilus, Filinia. Sub-order: Ploima Free-swimming, usually with ﬁrm lorica but some illoricate. Includes: Asplanchna, Brachionus, Kellicottia, Keratella, Notholca, Synchaeta, Trichocerca Phylum: Gastrotricha Minute unsegmented acoelomate metazoans. May be encountered in plankton of small freshwater bodies. Includes:Chaetonotus Phylum: Annelida Coelomate segmented worms. One class has planktic representatives. Class: POLYCHAETA Several planktic genera, one of which is very well adapted to a pelagic existence. Trochospere larvae of some polychaetes are also temporarily resident in the plankton. Includes: Tomopteris Phylum: Crustacea

Large group of segmented, jointed-limbed arthropods, with many planktic representatives. Class: BRANCHIOPODA Free-living small crustaceans with at least four pairs of trunk limbs, ﬂattened, lobed and fringed with hairs (phyllopods). Two orders have planktic genera. Order: ANOSTRACA Branchiopodans lacking a carapace, phyllopods numerous. Includes Chirocephalus, Artemia Order: DIPLOSTRACA Branchiopodans with a compressed carapace enclosing fewer than 27 pairs of phyllopods. Two sub-orders, one of which (Cladocera) includes several genera important in the plankton of sea and in lakes: Evadne, Podon (marine); Sida, Diaphanosoma, Holopedium, Bosmina, Daphnia, Ceriodaphnia, Moina, Simocephalus, Chydorus, Bythotrephes, Leptodora (freshwater) Class: OSTRACODA Free-living small crustaceans with a bivalve shell, few trunk limbs, none being phyllopods. Includes: Gigantocypris (marine), Cypris (freshwater) CONSUMPTION BY HERBIVORES 255

Ta b l e 6.1 (cont.)

Class: COPEPODA Free or parasitic crustaceans lacking carapace or any abdominal limbs. Of some seven orders, two provide most free-living planktic forms. A third is well represented in the benthos and species are encountered in the pelagic. Order: CYCLOPOIDEA Copepods with short antennules of <17 segments. Includes: Oithona (marine); Mesocyclops, Tropocyclops (freshwater) Order: CALANOIDEA Copepods with long antennules of >20 segments. Major group of mesozooplankters in the sea and in many lakes. Includes: Calanus, Temora, Centropages (marine); Eudiaptomus, Eurytemora, Boeckella (freshwater) Order: HARPACTICOIDEA Benthic copepods with similar thoracic and abdominal regions and very short first antennae. Includes: Canthocamptus (freshwater) Class: BRANCHIURA Crustacea, suctorial mouth, capacace-like lateral expansion of the head. Temporary parasites of fish. Includes: Argulus (freshwater and estuaries) Class: CIRRIPEDIA Crustacea, sedentary and plated as adults; wholly marine; several orders, one of which (Order THORACICA: barnacles) whose cypris larvae are dispersed in the marine plankton. Includes: Balanus Class: MALACOSTRACA Mostly larger crustacea, usually with distinct thoracic and abdominal regions. Thorax generally covered by a firm carapace; most abdominal segments bear appendages. Five major orders, two of which have typically planktic genera or ones whose juvenile stages are passed in the pelagic. Order: LEPTOSTRACA Primitive malacostracans with large thoracic carapaces. One genus is present in the bathypelagic beyond the continental shelf. Includes: Nebaliopsis (marine) Order: HOPLOCARIDA Benthic malacostracans with shallow carapace fused to three thoracic somites. Larvae are temporary entrants to the plankton of warm seas. Includes: Squilla Order: PERACARIDA Malacostracans in which the carapace is fused with no more than four thoracic segments. Several suborders include: Sub-order: Mysidacea Peracaridans with well-formed carapace. Mostly marine, ‘opossum shrimps’ are typically planktivorous in the deep layers of shallow seas. Some relict or invasive species in fresh waters. Includes: Leptomysis, Gastrosaccus (marine); Mysis (freshwater) 256 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Ta b l e 6.1 (cont.)

Sub-order: Cumacea Mostly benthic in marine sublittoral sand and mud, whence animals are entrained into pelagic samples. Includes: Diastylis Sub-order: Isopoda Peracaridans with a carapace covering three or four thoracic segments only. Most are not planktic. An exception is: Eurydice (marine) Sub-order: Amphipoda Peracarida with no carapace. Body laterally compressed. Most of the shrimp-like animals are littoral or benthic but some euplanktic genera. Includes: Apherusa (marine); Macrohectopus (freshwater genus of Lake Baykal) Order: EUCARIDA Malacostracans in which the capace is fused to all thoracic segments. Two main sub-orders:

Sub-order: Euphausiacea Eucarida in which the maxillary exopodite is small and the thoracic limbs do not form maxillipeds. Large meso- and macroplankters, including krill, important as a food for whales. Includes: Euphausia, Nyctiphanes (marine) Sub-order: Decapoda Eucarida in which the maxillary exopodite is large (the scaphognathite) and the first three pairs of thoracic limbs are modified as maxillipeds and the next five as ‘legs’. These are the lobsters, prawns and crabs. Zoea, megalopa and phyllosoma larvae are temporary entrants to the marine plankton. Includes: Carcinus, Palinurus Phylum: Arthropoda Class: HEXARTRA (INSECTA) Larvae of two orders show distinct adaptations to planktic existence. Order: MEGALOPTERA First (especially) and second instars of alder flies are dispersed in the limnoplankton. Includes: Sialis Order: DIPTERA Larvae of the Culicidae are typically associated with the littoral of lakes and many feed in very small, still bodies of water. Larvae of the subfamily Chaoborinae (or Corethrinae) are adapted for a larval life in the open, deeper waters of small lakes and lagoons. Phylum: Mollusca Includes: Chaoborus, Pontomyia

Unsegmented coelomates with a head, a ventral foot and a dorsal visceral hump, developed to varying extents. Of the ﬁve major classes, only two have typically planktic representatives. Class: GASTROPODA Slugs and snails. Molluscs with distinct head and tentacles. CONSUMPTION BY HERBIVORES 257

Ta b l e 6.1 (cont.)

Order: PROSOBRANCHIATA Gastropods in which adults show torsion. Some marine genera dispersed by pelagic trochophore larvae. Includes: Patella Order: OPISTHOBRANCHIATA Gastropod line showing secondary ‘detorsion’ and shell reduction. Several marine genera of pteropods or ‘sea butterﬂies’. Includes: Limacina, Clio Class: LAMELLIBRANCHIATA Bilaterally symmetrical molluscs more or less enclosed in a hinged bivalve shell. Certain genera dispersed by pelagic trochophore or veliger larvae. Includes: Ensis, Ostrea [trochophore] (marine); Dreissenia [veliger] (freshwater). Class: CEPHALOPODA Bilaterally symmetrical molluscs, with well-developed head, and foot modiﬁed into a crown of tentacles. Some marine pelagic species release paralarvae into the plankton. Includes: Loligo Phylum: Chaetognatha Slender, differentiated coelomates with distinctive head, eyes and chitinous jaws. Chaetognathes (arrow worms) are exclusive to the marine plankton, where they are carnivorous. Includes: Sagitta Phylum: Ectoprocta

Unsegmented sedentary coelomates, usually colonial. One division is exclusive to marine habitats and reproductive propagules are dispersed as trochophore-like cyphonautes larvae (freshwater ectoprocts produce dispersive statoblasts). Order: PHYLACTLAEMATA Marine ectoprocts producing planktic cyphonautes larvae. Includes: Flustra Phylum: Phoronidea Small group of unsegmented tubicolous coelomates with afﬁnities to the ectoprocts. The free-swimming actinotrocha larvae are encountered in the marine plankton. Includes: Phoronis Phylum: Echinodermata Large group of coelomates in which adults show radial symmetry. Modern genera are exclusively marine, usually littoral or benthic but many are dispersed by planktic larvae. One genus known to have planktic adults. Class: ASTEROIDEA Starﬁsh and seastars; pentagonal free-living benthic and littoral echinoderms. Many genera dispersed as pelagic bipinnaria larvae. Includes: Asterias 258 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Ta b l e 6.1 (cont.)

Class: OPHIUROIDEA Brittle stars; discoid free-living benthic and littoral echinoderms with ﬁve radial arms. Many genera dispersed as pelagic pluteus larvae. Includes: Ophiura Class: ECHINOIDEA Sea urchins; globular or discoid armless echinoderms. Many genera dispersed as pelagic pluteus larvae. Includes: Echinus Class: HOLOTHUROIDEA

Sea cucumbers; sausage-like, armless echinoderms. Many genera dispersed as pelagic auricularia larvae. One adult is bathypelagic in the South Atlantic Ocean. Includes: (larval) Holothuria, adult Pelagothuria Phylum: Chordata Coelomate animals with notochord and gill slits and possessing a dorsal hollow central nervous system. One ‘protochordate’ subphylum and the vertebrate subphylum have planktic representatives. Subphylum: UROCHORDA (TUNICATA). Unsegmented, boneless chordates, notochord restricted to larval tail. Class: ASCIDIACEA Sedentary tunicates. Motile, appendicularia larvae (‘ascidian tadpole’) has well-developed notochord. They enter and are briefly resident in the the marine plankton but do not feed. Includes: Ciona, Clavelina Class: THALIACEA Salps; pelagic tunicates of warm seas. Circumferential muscle bands are used to pump water through body, providing food and propelling animals forward. Tadpoles develop into zooids that are eventually set free as young salps. Includes: Doliolum, Salpa, Pyrosoma Class: LARVACEA Neotenic pelagic tunicates in which the appendicularian tadpole becomes the sexual form. These are planktic but live within a secreted ‘house’, which itself resembles a salp, and which is equipped with filter. The larvacean’s movements produces the filtration current. Includes: Oikopleura Subphylum: VERTEBRATA Chordates that develop an articulated, bony or cartilaginous backbone. Of the eight or so extant classes, only one is considered to have typically planktic representatives. Class: ACTINOPTERYGII Bony fishes. Many types of pelagic, marine demersal and limnetic littoral feeding fish grow either from pelagic eggs and larvae or from larvae hatched from eggs on the sea bottom. Initially, at least, the larvae are truly microplanktic.

Compiled from several sources: Hardy (1956), Borradaile et al. (1961), Donner (1966), Reynolds (2001b). CONSUMPTION BY HERBIVORES 259 and where feeding relies mainly on encounters ingesting so many gas vesicles that they became of food organisms by consumers, the availabil- irreversibly buoyant. The remarkable ability of ity of a substratum to which to attach does Nassula to ingest long filaments of green algae not necessarily improve feeding efficiency. The (Binuclearia)and Cyanobacteria (Planktothrix)by heterotrophic nanoflagellate genera Bodo, Monas, sucking them in, spaghetti-like, and coiling them Bicosoeca, Monosiga are represented by species in intracellularly (Finlay, 2001, and personal com- both the marine and the fresh water plankton. munication) provides a striking case of the feed- Other microplanktic protists include sar- ing adaptations of this animal. codines and ciliophorans, which may range in size between 10 and 200 µm. The radiolarians and Multicellular microzooplankton foraminiferans are mainly marine (though the Metazoans contribute to the composition of both latter are represented in fresh waters). Most are themarine and freshwater microzooplankton phagotrophic on detritus and picoplankters but but, despite some common features, the differ- radiolarians also harbour algal symbionts. Amoe- ences in the principal organisms represented are bae are not major players in the plankton, gen- substantial. In the sea, they are dominated by erally contributing <5% of the nanoheterotroph larval crustaceans (especially the nauplii of resi- biomass (Sorokin, 1999)butdense populations dent copepods), rotifers and larvaceans as well as are now recognised in the region of hydrother- thelarvae of other groups, such as molluscs and mal vents. echinoderms (see Table 6.1). There is a wide range Ciliophorans are often numerous and well of food preferences (nanoplanktic autotrophs, represented in the microplankton of lakes and heterotrophs and algae) as well as detrital parti- seas by some common and highly cosmopolitan cles. Cilia around the oral region, aided by mus- species (Finlay and Clarke, 1999;Finlay, 2002). cular contractions around the feeding apparatus, These include species of the naked spirotrichs or (in the case of rotifers and nauplii), mandibu- (such as Coleps, Strombidium, Strobilidium)and lar mouthparts may be used to handle captured holotrichs (Prorodon, Pleuronema), as well as the particles into the digestive tract but the main loricate Tintinnidium.Infreshwater,vorticellids feeding strategy is still largely encounter. Larger are epiphytic on large algae and use their oral microplankters may have some limited influence cilia to move particles into the cytostome. Micro- over orientation and exploration of the local envi- zooplankters feed principally on nanoplanktic ronment but, mostly, they are still too small autotrophs and heterotrophs, thus fulfilling a key to overcome the problem of viscosity. The lar- linkage in the transfer of carbon through the vacean, Oikopleura, perhaps comes closest to gen- microbial food web (Sherr and Sherr, 1988)(see erating and filtering a significant feeding current also Section 3.5.4). Ciliates may become the dom- through its secreted ‘house’ (see Table 6.1). inant animal in micraerophilous or anoxic sea The multicellular microzooplankton of lakes water (such as in the Black Sea, at depths >30 m) is often dominated by rotifers and copepod or in the metalimnia of eutrophic lakes (Fenchel nauplii. Feeding among the freshwater rotifers and Finlay, 1994). Other, mainly benthic or deep- has been studied extensively; the comprehensive waterciliates are frequently encountered in reviews of Donner (1966)andPourriot (1977) con- plankton samples from shallow water columns. tinue to provide helpful guides. Production of the Among fresh waters, planktic ciliates that most common pelagic rotifers in lakes (Keratella, feed on larger or more specialised foods some- Brachionus, Synchaeta, Polyarthra)responds well to times rise to become, usually for short periods, abundant populations of nanophytoplankton but dominant consumers of algae or cyanobacteria there is an evident selectivity which is influ- or flagellates (Dryden and Wright, 1987). Some enced by the size of the food organisms (Gliwicz, cases havebeenreported(Reynolds, 1975;Heaney 1969). For instance, the relatively robust Keratella et al., 1990)inwhichNassula effectively removed quadrata experiences an upper size limit of inges- thebiomass of floating Anabaena from the sur- tion of 15--18 µm but, for the smaller K. cochlearis, face layer of a lake, in one case the animals it is only 1--3 µm. Thus, it is hardly surprising 260 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

that, in the experiments conducted by Ferguson or littoral in distribution. Cyclops vicinus and Meso- et al. (1982), both species coexisted and were, cyclops leuckarti are species that are common and simultaneously, able to increase while in the widely distributed in the plankton of larger lakes. presence of a phytoplankton with abundant pop- Adult calanoids are more cylindrical, have ulations of Chlorella, Rhodomonas and Cryptomonas. long antennules which are extended laterally to However, only K. quadrata flourished among a sub- ‘hang’ on a rotational current generated by the stantially unialgal Cryptomonas nanoplankton. beating of the paddle-like thoracic limbs. The animal moves abruptly to a new position by a single Freshwater mesozooplankton beat of the antennules (Strickler, 1977). Calanoids The mesozooplanktic element (0.2--2 mm) are ablefeedonsmall(∼4-µm) algae and bac- embraces what are, to many people, the most terised particles which are filtered by bristle-like familiar components of the zooplankton. These setae on the maxillae from the same currents animals are big enough not just for their move- generated by the swimming appendages (Van- ments to escape the constraints of viscosity but derploeg and Paffenhofer,¨ 1985). The filtration for themtobeabletoexploitturbulenceandcur- ratesmay reach 10--20 mL per individual adult rent generation to optimise contact with poten- per day (Richman et al., 1980; Thompson et al., tial foods (Rothschild and Osborn, 1988). The 1982), although most reported averages are an groups of animals that are principally involved order of magnitude smaller. In addition, animals are really quite diverse and, beyond some shared feed on larger algae and ciliates, up to 30 µm adaptations, they are fitted to mutually distinct in size, which are actively captured and manip- life modes and fulfil different ecological roles. ulated with the maxillae and maxillipeds (and Any residual notion that zooplankton just eat probably other appendages too). Prior to making phytoplankton must be rejected as being crassly its strike, the animal will have detected and delib- oversimplistic! The common adaptations include erately oriented itself towards its quarry. The inci- the tendency to transparency (to minimise their dence of successful encounters is high (Strickler visibility to planktivorous fish, crustacea and and Twombley, 1975). Whether or not calanoids other potential predators) and the ability to should still be regarded as being primarily herb- propel themselves through the water. Individual ivorous, they have a demonstrable potential to adaptations concern their means of movement control the numbers of ciliates in the plankton and, especially, their means of gathering their (Burns and Gilbert, 1993; Hartmann et al., 1993). required food intake. The two feeding modes afford to calanoids an In most fresh waters, the mesozooplankton enhanced dietary flexibility, while the measure comprises crustaceans from two main classes (see of electivity allows them to survive lower concen- Table 6.1): copepods (from two orders in par- trations of food. ticular, the cyclopoids and the calanoids) and The cladocera are specialised filter-feeders. branchiopods (of the sub-order Cladocera). Adult The body is much modified from the basic crus- (final-instar) planktic cyclopoids are faintly pear- tacean form: a short thorax and abdomen car- shaped and streamlined with the paddle-like ries a compressed, shell-like carapace that forms thoracic legs held under the body. They have achamber in which four to six pairs of flattened, short biramous antennules and several caudal setae-bearing trunk limbs (‘phyllopods’) beat rami of varying lengths. Cyclopoids swim gently rhythmically. Their motion draws water through by reciprocation of the antennules and antennae thevariable carapace gape and the setae filter but they can ‘pounce’ as well, through the simul- particles from the inhalant current (Fryer, 1987; taneous use of the thoracic limbs. They are rap- Lampert, 1987). The animals swim by beating torial feeders (they seize their food) on a range the large, biramous antennae. Several cladoceran of nano- and micro-planktic particles including families are represented in the fresh-water plank- algae, rotifers and detrital particles. There are ton. The Sididae, which have six pairs of phyl- numerous species in several genera; many are lopods and strong, branched antennae, are found confined to ponds, some are primarily benthic mostly in vegetated margins and ponds. The CONSUMPTION BY HERBIVORES 261

Holopedidae are represented by a single genus, Moina species are most closely associated with which has a reduced carapace and is instead small water bodies with a tendency to offer suit- embedded in a mass of jelly. Bosminids are plank- able habitat conditions on a temporary basis tonic in ponds and small lakes and have a wide but explosive growth phases afford a dynamic geographical distribution. The macrothricid and advantage when favourable conditions obtain chydorid cladocerans have relatively small anten- (Romanovsky, 1985). In the open pelagic of perma- nae, and are mainly feeders on hard surfaces. Chy- nent larger lakes, dominance among the daph- dorus sphaericus is extremely common in the bot- niids is contested by such species as D. cucul- tom water and among weeds of small lakes and lata, D. galeata, D. hyalina and D. pulicaria (Gliwicz, it is frequently encountered in the plankton of 2003a). the water bodies in which they are present. In two other families, the polyphemids and the lep- Marine mesozooplankton todorids, the carapace is small and covers little The principal groups of mesoplanktic herbivores more than the brood pouch; planktic species of in the sea are the calanoids, the cladocerans Bythotrephes and Leptodora are macroplanktic (2-- and the thaliacean tunicates (the salps and their 20 mm) predators and do not comply with the allies) (Sommer and Stibor, 2002). In fact, the generalisation about cladoceran filter-feeders. calanoids are the most familiar and such tem- There is one further family, the Daphni- perate shelf-water species as Calanus finmarchius, idae, whose species can be extremely promi- Acartialongiremis, Temora longicornis and Cen- nent in limnoplankton and which plays a major tropages hamatus have long been regarded as the role in regulating the structure and function main food organisms of commercially important of lacustrine ecosystems. Daphniids have five surface-feeding fish, like herring (Clupea haren- pairs of phyllopods within the carapace and, like gus) and mackerel (Scomber scombrus). Accordingly, the sidids, have powerful swimming antennae. they have been studied in some detail (e.g. Hardy, They are efficient and more-or-less obligate filter- 1956; Cushing, 1996). A long-enduring under- feeders. They can remove all manner of foods on standing of a three-link food chain (phytoplank- the filtering setae, within defined size ranges. The ton--zooplankton -- fish) places the calanoids at upper limit is set by the width of the carapace the fulcrum between the harvest of fish the pri- gape (which is species-specific and varies with the mary producing phytoplankton. The relative pro- size of the animal). The lower limit is governed by portions of the respective annual production by the spacing of the phyllopod setae (Gliwicz, 1980; these three components also fitted well with the Ganf and Shiel, 1985). As will be further explored contemporaneous appreciation of the pyramidal below, individuals are able to filter such relatively Eltonian relationship, with an approximate 10% large volumes of water that, under favourable transfer of the energy acquisition at each trophic conditions, it is likely that a significant popula- level being transferred to the one above (Elton, tion of maturing daphniids may be able to filter 1927;Cohen et al., 1990). This paradigm was the entirevolume of a lake in a day or less. The seriously challenged by the realisation of how implications for their food organisms, and for the large a proportion of pelagic photosynthate is other organisms using the same food resource, transferred, as dissolved organic carbon, through and for those other microplanktic feeders that microbes and their microplanktic consumers to can be themselves be ingested by the daphniids ciliates (Williams, 1970;Pomeroy, 1974;Porter are formidable and complex. et al., 1979; Sherr and Sherr, 1988) (see also Sec- There is considerable further differentiation tion 3.5.4). of the habits, predilections and dynamics within On this basis, ciliate-consuming calanoids are the Daphniidae and within the type genus, Daph- already the fifth stage in the food chain. How- nia. Simocephalus, Ceriodaphnia and some of the ever, the close coupling of the components and larger Daphnia species (D. lumholtzi, D. magna)are the functional integrity of microbial food webs more common in ponds or at the weedy mar- (e.g. Simekˇ et al., 1999)areknowntoachievea gins of lakes than in the open water of lakes. high ecological efficiency of energy transfer (10-- 262 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

35%: Gaedke and Straile, 1994a). Even so, the real arelatively rich tissue content of ribosomal problem very often relates to the low supportive RNA, bringing with it a consequent high cell- capacity of the nutrient resources available and phosphorus content. This is, incidentally, the the low biomasses that can ever be maintained. major factor influencing the relatively low C : P Selectively browsing calanoids are simply the stoichiometries (averaging about 80 : 1) that are most efficient harvesters of the carbon flux. More- typical among these (Gismervik, 1997)andother over,arelativelylowfecundity and modest rate planktic cladocera (Elser et al., 2000). of investment in egg production enables them to The third main group of marine meso- satisfy their minimum food requirements at low planktic animals comprises the pelagic, free- POC concentrations, in the range of 5--80 µgC living tunicates, especially the salps, pyrosomans L−1 (Hart, 1996) (as algae, this is roughly equiv- and doliolids that represent the Thaliacea (see alent to a chlorophyll content in the range 0.1-- Table 6.1). These near-transparent, gelatinous ani- 1.6 µgchla L−1). Except when food resources are mals have a low body mass, comprising little truly limiting, the dynamics of calanoid growth more than an open barrel-shaped tube, a filter- are most likely to be governed by temperature ing gill and circumferential muscle bands whose (Huntley and Lopez, 1992). It is even possible systematic contraction and relaxation refresh the that the distinctively oceanic calanoids (such as current of water across the filter screen. All Acartia clausi, Centropages typicus) function at yet pelagic tunicates are filter-feeders, straining per- lower resource availabilities than the shelf-water haps the entire nanoplanktic--microplanktic size species. range of particles (Sommer and Stibor, 2002). In the more enriched coastal waters, receiving In additon, they are, collectively, ubiquitous nutrient inputs from rivers or as a conequence of components of the pelagic fauna, from coasts deep-oceanic upwellings, several resource-driven to the deepsea;however,theyareperhapsbest effects are evident. There are absolutely more of known for their presence in the plankton of the biomass-constraining nutrients (N, P, Fe), at warm,ultraoligotrophic oceans. The low body once raising the potential to support more pri- mass requires absolutely modest resources for mary producers and to maintain a higher algal maintenance, while they expend little energy in biomass. The additional nutrients may also allevi- keeping their near-isopycnic structures from sink- ate the dependence of large algae upon turbulent ing. The architecture and physiology of these ani- diffusivity to fulfil their nutrient demands (cf. mals is substantially geared to function at very Riebesell and Wolf-Gladrow, 2002)(seealsoSec- low concentrations of assimilable POC. tion 4.2.1). There may well be a lowering effect on the Si--N and Si--P relationships, which some con- Planktivorous macroplankton, megaplankton sider relevant to changes in the species composi- and nekton tion of the phytoplankton, although these really Although this section has so far, taken a ‘bottom- depend on the absolute nutrient levels (Sommer -up’ view of the structure of the zooplankton, and Stibor, 2002). in emphasising the nature of the resource base The combination of these effects results and the evolutionary adaptations of the main in potentially greater concentrations of high- pelagic groups to be able to exploit it, it is quality, primary foods that will support direct only half the story. For, as many authorities filter-feeding. It is not just the fact that cladocer- tirelessly point out (e.g. Gliwicz, 1975, 2003a; ans, such as Evadne, Podon and Penilia, can filter Banse, 1994), active net production of each of the more water and, thus, harvest more food than components of the plankton of seas and lakes calanoids (Sommer and Stibor, 2002). They also is regulated by its consumers. Thus, the abun- have faster rates of metabolism and growth, with dance of ciliates in the open plankton might be proportionately more of their greater energy expected to increase on an abundant resource of intake (60--95%) being invested in partheno- nanoflagellates but the capacity to do so may be genetic reproduction (Lynch et al., 1986;Stibor, severely constrained by the numbers of calanoids 1992). At the physiological level, this requires or other predators (see, e.g., Thouvenot et al., CONSUMPTION BY HERBIVORES 263

2003). Equally, the growth of microphytoplank- tant euphausids. The latter are entirely pelagic ton inalakemightbeconstrained by the feed- throughout their lives; they live in all the oceans ing of herbivorous Daphnia but the vulnerability but the key place of Euphausia frigida and E. tri- of Daphnia to consumption by planktivorous fish cantha in the southern oceans is renowned for might not only reduce their impact upon the their being the main food of the great baleen phytoplankton but the latter would be allowed whales. Quantitatively less important are the car- to increase to something like its ungrazed nivorous crustacean larvae of decapods (crabs, potential. Such dynamic ‘cascading’ interactions lobsters) and of the mantis shrimps, Squilla spp. (Carpenter et al., 1985)maynowseemtobeself- celebrated by Hardy (1956)asbeing the ‘most evident phenomena but they were not formally beautiful of larvae’. Among fresh waters, non- described before the publication of now-classic vertebrate planktivores other than mysids occur quantitative studies of Hrba´ˇcek et al. (1961). Since mainly in inshore waters, and include larval then, trophic cascades and their manipulation megalopterans, hemipterans (e.g. Notonecta)and have been studied in great detail (see Carpen- dipterans. ter and Kitchell, 1993)andexploited as the basis Among the larger pelagic animals (fish, of system management by what has become squid), size and muscular strength take them known as biomanipulation (Shapiro et al., 1975; out of the plankton and into the swimming nek- see also Section 8.3.6). For the moment, however, ton. For these to be truly pelagic planktivores, Iseekonlytomakethepoint that the effects the ability to sample large volumes of water of mesoplanktic herbivory and microphagy on and strain from this food items of only 1--2 mm the dynamicsandstanding crops of the primary is essential and demanding of a very efficient producers are subject to cascading impacts of means of food filtration. In the herring and some planktivory. Again, the point is elegantly made other closely related clupeoid species, for exam- in Gliwicz’s (2003b)observation that the struc- ple, this capacity is provided by gill rakers -- tural composition and size distribution of the comprising numerous, long and slender close- zooplankton is very different between systems set bristles borne on the gill arches. The bask- with and without the presence of zooplanktiv- ing shark, Cetorhinus,isarelatively very large orous fish. The point is especially pertinent, as elasmobranch but its gill arches are analogously zooplankters have nowhere to hide in the open set with many close-set, flattened strips that water: survival depends on not being seen or function analogously to the rakers of bony fish eaten by planktivorous cosumers. Apart from (Greenwood, 1963). The direct sustenance of a the protection that comes from fortuitously low creature attaining a length of 10--12 m and a predator densities, much depends upon either body mass of several tonnes through feeding on being less visible (which exacts a premium on animals individually ten thousand times smaller zooplankton that might grow larger) or less acces- and 10−9 of its body mass is a truly impressive sible to visual predators by descending to the example of emergy gain through trophic link- lightless depths. The need to return to the surface age. In another, fresh-water case, the produc- waters to feed (at night!) invokes an unavoidably tive basis of the fisheries of the meromictic rift high energetic cost. valley Lake Tanganyika, founded mainly on two Besides adult fish such as herring and mack- species of planktivorous clupeid (Stolothrissa tan- erel (see above), marine consumers of mesozoo- ganicae, Limnothrissa miodon) and their endemic plankton include invertebrates of the next two centropomid predator (of the genus Lates:Lowe- size divisions -- macroplankton (2--20 mm) and McConnell, 1996, 2003), has been shown to be megaplankton (>20 mm). Among the most sig- quantitatively dependent upon the pelagic food nificant of these are the chaetognaths (arrow webofthe lake (Sarvala et al., 2002). Yet more worms), ctenophores (sea combs and sea goose- remarkable is the fact that the annual stim- berries) and the polychaete Tomopteris. There is ulus for production in this oligotrophic lake also a variety of crustaceans at this scale -- the relies heavily upon the recycling of nutrients mysids, the pelagic amphipods and the impor- during the period of increased wind action and 264 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

monimolimnetic deepening and the enhanced 6.4.2 Impacts of filter-feeding on production of picoplanktic cyanobacteria. Bacter- phytoplankton ial consumption of primary DOC yields between Moving on from qualitative description of the − − 25 and 130 g C m 2 a 1 to the pelagic food web, structural components of the phagotrophic which, in turn sustains the producton of up to plankton, consideration is now given to the quan- − − − 23 g copepod C m 2 a 1. Much of this (16 g C m 2 titative impacts of their feeding on the pro- − a 1)iseatenbyplanktivores in generating the net ducer mass. It is conceptually easier to deal first − − annual production of 1.1 g C m 2 a 1 Stolothrissa with the impacts of filter-feeders. Although this − − plus Limnothrissa and 0.3 g C m 2 a 1 Lates. method of food gathering is far from universal, Adults of many families of fish will eat zoo- it can be the most striking and complete in its plankton when it is sufficiently abundant to be impact. Moreover, its effects are relatively easy to an attractive and satisfying resource. The major- model. These are good enough reasons to explain ity of adult pelagic fish (and of many that inhabit the additional fact that a large literature on filter- shallower margins) are carnivorous on other fish feeding has accumulated. and/or on other large prey. However, many of Supposing that, to the potential planktic these species produce large numbers of small consumer, the relatively most abundant food eggs that give rise to juvenile stages, which are resource is the nanoseston -- algae, large bacteria, initially mesoplanktic. They feed on microplank- detrital particles measuring 2--20 µm across -- and ton (Sarvala et al., 2003), often in direct compe- that particles are generally well dispersed within tition with and exposed to predation by adult themedium, then the development of some planktivores (e.g. O’Gorman et al. 1987). Accord- means to sieve and to concentrate such parti- ing to the systematic simulation modelling of cles is likely to be favoured by evolution (Gliwicz, Letcher et al. (1996), metabolic growth capacity, 2003a). The coupling of a filter and the means rather than foraging ability or resistance to of generating a water current across is a char- starvation, is the leading bottom--up component acteristic of the feeding apparatus of many zoo- in larval survival. Predator size is a powerful plankters, including ciliates and rotifers. How- influence on survival but has only a weak effect ever, it is at the mesoplanktic scale, of crus- on the variability in the composition of the taceans and tunicates, that filter-feeding has a available prey. Letcher et al. (1996)also deduced significant impact on the availabilty of food in that whether young fish died through starvation the entire medium, or at least beyond the imme- or predation usually depended most on the diate environment of the individual animal. This availability of their smallest prey organisms. difference is most due to viscosity. Where the Reference should also be made to pelagic smallest turbulent eddy is in the order of 1 squid (Loligo spp.) whose juvenile hatchlings (or mm or so, the typical microplankter (<200 µm paralarvae) are released into the open water. in length) experiences a wholly viscous environ- They are free-living and self-propelling, using ment in which to move itself and, more impor- rhythmic contractions of the mantle to force tantly, to influence the encounter with particles aseriesofalternating bursts of water flow ≤20 µm. An analogy that comes to mind is of and recovery. Being barely 2 mm in length, a human trying to collect bananas while both paralarvae are, unmistakeably, initially (albeit are immersed in a swimming pool filled with a briefly) mesoplanktic (Baron,´ 2003). liquid having the consistency of molasses or set- On the basis of this brief survey, it is clear ting concrete. Scaling upwards, the same human that the precise structure of the pelagic web would be rather more successful in picking out of consumers is highly variable and subject to kidney beans from the same liquid but now dis- dynamic forces. So far as the impacts upon the persed in a vessel the size of a bath tub. It is only phytoplankton is concerned, outcomes hinge on by being big enough and strong enough to over- the numbers and sizes of the herbivores present come frictional drag and to generate turbulent and the sustainability of the feeding modes currents that it is possible to increase the rate of available. particle contact (Rothschild and Osborn, 1988). CONSUMPTION BY HERBIVORES 265

Quantitatively, the best studied of the three characteristic mesozooplanktic groups of filter- feeders is the Cladocera and, especially, those of the fresh-water genus Daphnia.Collectively, these also illustrate well the factors that most influence thedynamic impacts on the microplanktic food organisms: how many feeders there are, what and how much food they remove, and what the consequences might be, both for themselves (in terms of biomass increase) and for the food (in terms of how much more cropping it can withstand). Each of these components is pursued exhaustively in theavailable literature. Much of this amplifies the findings of some of the earliest of the modern investigations. Indeed, many of these were of such enduring quality that they provide an ideal base for this section.

Filtration rates Certainly for the larger individual filter-feeders, the basic quantity of interest is the volume of water that animals are able to strain per unit time. The usual means of its determination is to measure the rates of depletion from known Figure 6.4 Functional responses of (a) filtering rate and (b) feeding rate of filter-feeding animals with respect to food concentrations of radio-labelled ingestible foods. concentration. The arrow defines the incipient limiting To obtain sensible results in a short period of concentration, as defined by McMahon and Rigler (1963). time, it is necessary to make the measurements Redrawn with permission from Gliwicz (2003a). on suspensions of known numbers of animals, which, in turn, necessitates that the per capita volumes of water processed are nearly always mals that are ‘starved’ for some hours before mean values. Moreover, as the individual volumes introduction into a suspension of radio-labelled filtered vary conspicuously with the size of the food organisms. In this case, what is measured animal, it is necessary always to pre-sort the ani- is strictly the ‘particle clearance rate’. If all the mals beforehand. Possible methodological short- above conditions are satisfied, the mean indivi- comings attach to the effects of handling on the ual clearance rate should coincide with (but not animals’ performances. Another potential diffi- exceed) the mean volume of water processed per culty that must be addressed is that the removal unit time, which is the mean individual ‘filtra- of radio-labelled particles is incomplete or is tem- tion rate’ (F). The rate at which food particles are porary (i.e. food is selected or rejected, leading captured is obviously dependent upon the filtra- to an underestimate of the volume filtered). Fur- tion rate but the ‘feeding rate’ (or ‘ingestion rate’) ther, allowance has to be made for the possibilty is a proportion of the food concentration in the that, once satiated, the individual may slow its inhalant volume. Moreover, it has been demon- filtration rate. strated (McMahon and Rigler, 1963)that, at high Experience has shown that all these are real concentrations of food, clearance rates of Daph- constraints. Consensus has clarified their magni- nia slow down as the animals are sated for less tude and also spawned a terminology. All mean- filtering effort. The relationships between filtra- ingful measurements take place at known tem- tion and feeding as a function of food concentra- peratures and within short, timed exposures tion are sketched in Fig. 6.4.Belowthe‘incipient to known concentrations of size-categorised ani- limiting food concentration’, Daphnia is likely to 266 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

−1 Ta b l e 6.2 Individual filtration rates, Fi (in mL d ), for various planktic animals as reported in, or derived from relationships in, the literature

Species Fi References Rotifers Generally 0.02–0.2 Pourriot (1977) Brachionus calyciﬂorus 0.1–0.2 Halbach and Halbach-Keup (1974); Starkwether et al.(1979) Freshwater calanoids Eudiaptomus gracilis (12 ◦C) 0.6–1.8 Kibby (1971) Eudiaptomus gracilis (20 ◦C) 1.3–2.5 Kibby (1971) Eudiaptomus gracilis (adults, 17 ± 3 ◦C) 0.5−10.7 Thompson et al. (1982) (copepodites, 17 ± 3 ◦C) 0.5–6.7 Thompson et al. (1982) Diaptomus oregonensis (adults, 2.4–21.6 Richman et al. (1980) temperatures various) Freshwater cladocerans Bosmina longirostris <3.0 Thompson et al. (1982) Chydorus sphaericus 0.5–2.6 Thompson et al. (1982) Daphnia galeataa (<1.0 mm, 17 ± 3 ◦C) 1.0–7.6 Thompson et al. (1982) (1.0–1.3 mm, 17 ± 3 ◦C) 3.1–19.3 Thompson et al. (1982) (1.3–1.6 mm, 17 ±3 ◦C) 3.1–30.7 Thompson et al. (1982) (1.6–1.9 mm, 17 ± 3 ◦C) 14.0–60.0 Thompson et al. (1982) Daphnia spp. (<1.0 mm, 15–20 ◦C) <5.0 From Burns’ (1969) regression (1.0–1.3 mm, 15–20 ◦C) 3.6–10.4 From Burns’ (1969) regression (1.3–1.6 mm, 15–20 ◦C) 6.4–18.6 From Burns’ (1969) regression (1.6–1.9 mm, 15–20 ◦C) 10.1–30.1 From Burns’ (1969) regression

aThe organism was reported as D. hyalina var. lacustris. Under current nomenclature, the identity D. galeata is to be preferred (D. G. George, personal communication).

be hungry (‘food-limited’) and to filter-feed as fast The superior filtration capacity of Daphnia as it is able. (especially larger individuals) is explicit in the It was another of Frank Rigler’s colleagues, relationship that Burns (1969) demonstrated Carolyn Burns, who made some of the first accu- between the filtration rates (Fi)offour species rate measurements of the filtration rates in Daph- of Daphnia (D. magna, D. schoedleri, D. pulex, D. nia.Herwork(Burns 1968a, b, 1969) has been well galeata)and their carapace lengths (Lb). The plots supported by subsequent determinations by oth- in Fig. 6.5bandtheentries in Table 6.2 are calcu- ers (e.g. Haney, 1973;Gliwicz, 1977; Thompson lated from her regressions. The measurements of et al., 1982), to the extent that her original Thompson et al. (1982)onD. galeata are especially detailed findings are used for this quantitative well predicted. At 15 ◦C, the hourly filtration rate development. What remains remarkable is the is given by enormous capacity of the feeding current created 2.16 by the rhythmic beating of the thoracic limbs to F i = 0.153L b (6.11) draw water into the carapace chamber and across the filtering setae on the third and fourth tho- and at20◦C racic limbs. Comparison with other zooplankters 2.80 is made in Table 6.2. F i = 0.208L b (6.12) CONSUMPTION BY HERBIVORES 267

Figure 6.5 Filter-feeding in Daphnia spp. (a) The maximum volume of water ﬁltered by animals, also as a function of body length, at two temperatures (data of Lampert, 1977a); (b) The size of the largest particle available to an individual animal as a function of its body length, Lb, according to Burns (1968a). Figure redrawn with permission from Reynolds (1997a).

Possibly the most pertinent deduction is the fact range of potential foods of filter-feeding cladocer- that as few as 20 large Daphnia per litre of lake ans increases with the maturity of the consumer. water, or 200 neonates L−1,issufficient a popula- Whereas a 1.0-mm Daphnia is probabilistically tion to process daily the entire volume in which restricted to foods <25 µminsize, a 2.0-mm ani- they are suspended. More generally, the aggre- mal can take food particles up to 50 µm across. gate volume of water that is potentially filtered Conversely, for smaller animals the food availabil- each day ( Fi)isequivalentto: ity may be rather more restricted and the feeding rate falls below the potential of the filtration F = (N · F ) + (N · F ) +·····(N · F ) (6.13) i 1 i1 2 i2 i ii rate. Those items that are too large are simply where F ii is the filtration rate and Ni is the stand- rejected and do not enter the filter chamber. As ing population of the ith species size category. Gliwicz (1980)recognised, the filtering daphniid is very easily able to regulate the size of food par- Food availability ticle that reaches the phyllopods through its con- The lower end of the size range of particles trol over the carapace gape. Obviously it cannot available tothefilter-feeder is determined by accept particles above a size-specific maximum the filter itself. In the case of the daphniids, (Gliwicz and Siedlar, 1980)butitmay,however, it is set by the spacing and orientation of the self-impose a lower maximum, perhaps to avoid setules, the short branches besetting the filter- ingesting mucilaginous colonies. Thompson et al. ing setules fringing the third and fourth tho- (1982)observed sharply reduced filtering rates racic phyllopods (Gliwicz, 1980;see also Gliwicz, of D. galeata when the phytoplankton was dom- 2003a,andreferences cited therein). Comparing inated by Microcystis colonies of varied size. The this character with the filterable particles recov- possibility that the behaviour was in some way ered by rotifers, calanoids and other cladocerans attributable to toxicity of the phytoplankter (Geller and Muller,¨ 1981;Reynolds, 1984a), there seemed a less likely explanation than the direct seems to be little interphyletic variation, 0.2--2.0 observation that the rate of phyllopod beating µmbeing a general value. In fact, the efficiency was impairedonlyifaMicrocystis colony became of retention of the smallest particles may be low- ensnared in the apparatus or blocked the median ered in Daphnia,owingtosome leakage from the chamber. At this point, the post-abdominal claw filter, from the median chamber and the food was flexed and used to scrape out the blocking groove, before they get to the animal’s mouth. mucilage. Thompson et al. (1982)argued that so Fewer particles in the range 1--3 µmareretained many animals were spending so long purging the than in the range 5--10 µm(Gliwicz, 2003a). filtering apparatus that the aggregate filtration The upper size limit of particle that can be rate became severely depressed. ingested is, according to Burns (1968a), strongly It is not just the size and texture but the correlated to animal size (Fig. 6.5b). The relation- shape of the phytoplankton that influences the ship makes the important statement that the proportion of food strained from the filtration 268 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.6 Schematic representation of food selectivity in Daphnia pulicaria (vertical arrows indicate food items retained, side arms show those lost or rejected) at three critical points in the feeding process. (a) Encounter and intake into the ﬁlter chamber; (b) capture from phyllopods to food groove; (c) ingestion of particles at the mouth. From an original representation of Hartmann and Kunkel (1991), redrawn with permission from Gliwicz (2003a).

current. This topic was elegantly investigated and All these facets contribute to feeding rates summarised by Hartmann and Kunkel (1991). The that are below (in some instances, well below) diagram in Fig. 6.6 distinguishes the progress to thepotential of the aggregate filtration rate. ingestion of three differing algal shapes. Small Reynolds et al. (1982a)proposed a food-specific sphaeroid and cuboidal unicells are easily drawn correction factor (here designated as ω)inorder in to the median chamber and efficiently com- to relate removal rates to aggregate filtration rate pacted by the phyllopods, and most of that food (F). As removal of algae from the water is recip- will be ingested. Slender algal cells are more dif- rocated by the random redispersion of the sur- ficult to orientate and compress and there is vivors in ostensibly the same volume of water, some loss from the median chamber and some thereaction of the extant algal population corre- rejection from the food groove. Long filaments sponds to another exponential series, analogous are really quite difficult. However, as observed to dilution (cf. Eq. 6.7). The analogous grazing loss by Nadin-Hurley and Duncan (1976), Daphnia is rate term, rG,inflicted upon the algal population able to arrange foods into spaghetti-like bun- is given by dles (though not without significant rejection losses). rG = ω (F i)/V (6.14) CONSUMPTION BY HERBIVORES 269

Thompson et al. (1982)found that the removal of thestatus of a number of cyanobacterial genera nanoplanktic unicells and Cryptomonas from the has been puzzling. Work with pure cultures led feeding current of D. galeata is highly effective, Rippka et al. (1979)totake a strongly reductionist so that the value of ω is close to 1 and rG is view of cyanobacterial diversity, proposing that little different from that predicted directly from asmall number of named genera could accom- the filtration rate. The value of ω falls to ∼0.3 modate the few essential distinctions among the foreight-celled Asterionella colonies and rapidly unicellular strains (size, shape of cells and planes from ≤0.3 to zero for Fragilaria colonies com- of cell division). Since then, new techniques and prising more than 6--13 cells per colony. Large anew generation of researchers have scarcely Daphnia are capable of feeding on small Eudorina added to the range of known picocyanobacteria. colonies, short Planktothrix filaments and young Most known inland-water forms conform to being Microcystis colonies while they are still quite small short rods (Synechococcus), ellipsoids (Cyanobium) (m generally <50 µm) but have great difficulty or spheroids dividing in one or two planes with larger colonies. Thus, the rate of removal, (Cyanothece)(Komarek,´ 1996;Callieri and Stockner, rG,variesamongthealgaein mixed populations, 2002). Moreover, the similarity of the cells of even when they are simultaneously subject to those of various species of colonial genera the activities of the same set of filter-feeders. inhabiting mildly eutrophic waters (such as Combined with the age--size structure of the Aphanocapsa, Cyanodictyon and Synechocystis) has filter-feeding populations, precise values of rG are been noted on many occasions and attribution scarcely easy to calculate and should carry such to the same or close genetic lines has been awide margin of error that, for most purposes, proposed. The experiments of Komarkov´ aand´ it is acceptable to work with approximations. It Simekˇ (2003)imitated transformations of grow- should also be borne in mind also that if vertical ing strains of colonial Aphanocapsa and Synechocys- migration takes the main filter-feeding compo- tis into unicellular suspensions, and back, stimu- nents of the zooplankton to depths beyond the lated by the presence or absence of herbivorous visibility of fish, and they return to the alga-dense brine shrimp Artemia (or to chemicals in medium surface waters only during darkness, then Eq. in which Artemia had been present). (6.14)isyet more difficult to evaluate. The maxi- Interestingly, this behaviour mirrors the mum filtration rates of Daphnia are no higher by known morphological anti-predator defences night than by day (Thompson et al., 1982). (lengthened spines, bulbous heads) that are Before concluding this section, it is also inducible in cladocerans and rotifers exposed important to make reference to the adaptations to water in which fish or even Chaoborus lar- that algae invoke to make themselves less palat- vae have been present (see Gliwicz (2003a)fora able to the filter-feeding consumers with which detailed overview of the literature). Chemosen- they do come in contact. In mathematical terms, sory perception in locating and selecting prey these help them to reduce the instantaneous is probably vital in the viscous world of micro- value of ω.HessenandvanDonk(1993) observed zooplanktic consumers and the capability may atendency of some species of alga to main- well be widespread among the planktic protists tain larger coenobia (sensu more cells per coeno- (Weisse, 2003). It is reasonable to expect that bium) in the presence of Daphnia than without. chemoperception works in the opposite direc- They showed experimentally that growing clones tion and that predator detection and reaction of Scenedesmus maintain higher proportions of is similarly influenced. The ciliate Euplotes is colonies comprising eight or more cells in media known to react to predator-specific chemical fac- in which Daphnia had been present but since tors produced by its amoeboid predators by pro- removed. Their findings have been repeated by ducing giant, uningestible cells (Kusch, 1995). The Lampert et al. (1994). chemical nature of the substances involved is Another interesting discovery is the reaction not well known. They are collectively referred of picoplanktic cyanobacteria to the presence of to as kairomones, though their mutual similari- grazers. On strict grounds of cell morphology, ties owe to the ability of potential prey to sense 270 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

the threat of potential predators, and not to any (1983), working with Eudorina,found that larger known chemical likenesses. The production of colonies escaped ingestion and uncropped colony kairomones is distinct from the production of growth and recruitment were such to explain the overtly toxic substances by potential prey, whose dynamics of population increase. It could be said effects on would-be consumers may be quite gen- that, by removing smaller algae, larger units are eral or incidental unintentional in their effects positively selected by moderate aggregate filtra- on consumers. The distinctions blur somewhat tion rates. in the interesting interrelationship between the toxin-producing mixotrophic haptophyte Prymne- Algal removal and grazer nutrition sium and its phagotrophic dinoflagellate preda- Even a broad picture of the effects of filter- tor, Oxyrrhis.According to Tillmann (2003), when feeding on the resource cannot be completed Oxyrrhis wasintroduced into dense cultures of P- without reference to the dynamic limits of filter- limited Prymnesium,itsinitial feeding rate was feeding activity, or to the way that this changes quickly depressed (to <0.1 cell grazer−1 h−1) through time. The answers to both problems below that of control animals fed on similar- depend upon the relation of nutrition, growth sized cryptophytes (2.75 cells grazer−1 h−1), a and recruitment of the consumers and the quan- direct response to toxicity. Poisoned Oxyrrhis cells tity and quality of the food available. The food then lysed and were attacked by phagotrophic requirements of Daphnia pulex were exhaustively Prymnesium,reversing the direction of the carbon investigated by Lampert (1977a, b, c). He first flow! The Prymnesium-free medium also invoked derived equations to describe the maximum lysis in Oxyrrhis,though the effect reduced when hourly assimilation rates of Daphnia,asafunc- the Prymnesium culture was more dilute or the tion of the length (Lb)andmass (wb)ofindivid- Oxyrrhis were more abundant. ual animals at various temperatures. At 15 ◦C, a Many green algae, Cyanobacteria and some 0.8-mm neonate assimilates up to 2.4 µgCd−1, chrysophytes are normally invested in mucilagi- whereas a 2.1-mm adult is accumulating at 15.7 nous sheaths. Among many other functions that µgCd−1. The amount of food needed to supply mucilage might serve (see Box 6.1), the pack- such requirements varied with the quality of the age increases the size of the algal particle and food. The highest assimilation efficiencies (∼60%) decreases the likelihood of its entry into the fil- came on such readily filterable and digestible ter chamber of Daphnia,orits retention on the algae as Asterionella and Scenedesmus. Thus, to sati- filter or its successful ingestion. Thompson et al. ate the metabolic capacity requires the feeding (1982)founddepressed values of ω for Daphnia to yield upwards of 4.0 and 26.2 µgCd−1 (to the feeding on Eudorina colonies, except those newly smaller and larger animal respectively). On the released daughters being <25 µmindiameter. other hand, the respirational expenditure for the Even if they are ingested, mucilaginous colonies same individuals (respectively, 0.6 and 4.3 µgC are resistant to digestion. They are not only d−1)defines the minimum daily intake that will capable of viable passage (see Canter-Lund and just maintain metabolism, below which they will Lund, 1995 for examples) but they are said to lose weight and eventually die of starvation. use the opportunity of exposure to high nutri- The volume of water that can be filtered ent concentrations to absorb and store them and defines the external food concentrations that will to use them effectively after release from the sustain the minimum and saturation require- anus (Porter, 1976). Gliwicz (2003a) considered ments of the Daphnia.From the appropriate that, despite doubts about the extent of diges- entries in Table 6.2,itisunlikely that a 0.8-mm tive resistance, the net profit of nutrient uptake D. pulex might filter more than 5 mL of lake water by algae surviving gut passage might well com- each day, while the 2.1-mm animal may be capa- pensate. This might explain the frequent observable of procesing 30 mL. Then the minimum con- tion that the numbers of mucilaginous colonies centration of filterable food necessary to fulfil the often increase when the density of filter-feeding neonate’s minimum requirement is thus 0.6 µg Cladocera is high. However, Reynolds and Rodgers Cper5mL, i.e. ∼0.12 µgCmL−1;however,a CONSUMPTION BY HERBIVORES 271

Box 6.1 On the sticky question of mucilage

Sheaths or investments of mucilage are produced characteristically around the cells of many kinds of planktic algae and bacteria, often binding them in colonial structures (as in chroococcoids such as Microcystis,insulphur bacteria, among representatives of several orders of chlorophyte, chrysophyte and haptophyte). Mucilage also covers filamentous Cyanobacteria (Anabaena, Planktothrix) and some unicellular algae, including certain diatoms. Mucilaginous threads are trailed by Thalassiosira filaments and, possibly, by many other kinds of planktic alga (Padisák et al., 2003a). It is a feature of both marine and freshwater species. Mucilage investments vary in texture, from being robust and readily visible under the light microscope (e.g. Microcystis wesenbergii)tobeing, as in some desmids, so tenuous to require negative staining in (e.g.) Indian ink preparations to reveal the existence as a translucent halo around the organism (John et al., 2002). On other occasions, the extent of a mucilaginous sheath is identifiable under the microscope by the numbers of bacteria and detrital particles that cling to the perimeter. Despite the ubiquitous occurrence of algal mucilage and the fortuitous assistance it gives to microscopists attempting to deduce the identity of the organisms they encounter, there are surprisingly few general accounts in the literature that consider the functions and benefits that mucilage might provide or that question how the many other species of alga seem to manage quite well without it. The probability is that there is no consensus answer anyway. There are certainly several measurable benefits that the presence of mucilage imparts to the organisms that produce it. These are considered in detail at appropriate points in this book. However, it has not been resolved that any of these is a primary or an original function of mucilage production or merely opportunistic adaptive applications of some ancient trait. Mucilages (the plural is probably reasonable) are hygroscopic lattice-like polymers of carbohydrate and substances resembling acrylic. In the literature, the product is sometimes referred to as mucus, though this term is generally applied to similar polysaccharides produced in many groups of animals (especially coelenterates, molluscs, annelids and many kinds of vertebrate). The elemental composition (C,H,O) of the secretions involves little of intrinsic value and, in this sense, may be considered as a by-product of metabolism. The observation has been made (Margalef, 1997) that there is little difference biochemically between producing mucilage and any other unused extracellular photosynthetic derivative, save that mucilage is not released in solution. The possibility that mucilage production originated as a mechanism for regulating the accumulation of photosynthate in cells that cannot be assimilated into amino acids and proteins has some resonance with statements suggesting that mucilage-bound algae are more common in nutrient- poor waters than in enriched systems and that organisms that produce variable amounts of mucilage (such as Phaeocystis) produce more when nutrient (especially phosphorus) concentrations are depleted (Margalef, 1997). The production of gelatinous polysaccharides has been observed among marine phytoplankton populations in the photic layer that have become ‘aged by nutrient deficiency’ (Fraga, 2001, citing Vollenweider et al., 1995; Williams, 1995). Margalef (1997) makes the 272 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

point that mucilage production is more frequent over long days and in shallow mixed layers. This, too, might be indicative of causal imbalances in the intracellular metabolism of carbon, nitrogen and phosphorus. Mucilage certainly has a high water content and, in some cases, it must disperse rapidly into the medium (whilst being replaced by secretion from the proximal side). In spite of the high density of the polysaccharide, the mean density of the mucilage in live Microcystis colonies is within 0.07% of the density of the water in which they are suspended (Reynolds et al., 1981) (see Section 2.5.2). This has for long nurtured the supposition that mucilage contributed to the suspension of phytoplankton by reducing average density. This it certainly can do, but it is not effective in reducing sinking rate unless the overall dimensions comply with Eq. (2.17) (Hutchinson, 1967;Walsby and Reynolds, 1980). Other functions proposed to be fulﬁlled by mucilage include the following.

Streamlining Almost in direct contradiction to the principle of reducing sinking rate, a large mucilage investment enhances ﬂoating and sinking responses to self-regulated buoyancy changes in colonial Cyanobacteria such as Microcystis and Woronichinia, making controlled migrations in natural water columns feasible (See pp. 68, 81).

Nutrient storage The mucilage has been supposed to provide a repository for the concentration and storage of essential nutrients (e.g. Lange, 1976). No mechanism for this has been suggested; it is not clear how outward diffusion gradients and progressive dilution and dissipation of the mucilage effects could be countered.

Nutrient sequestration and processing In nutrient-dilute environments, encounter with sufficient limiting nutrients is an empirically demonstrable problem (Wolf-Gladrow and Riebesell, 1997) (see Sec- tion 4.2.1). It is possible that a mucilaginous coat provides a cheap mechanism for increasing the size of the algal target whilst simultaneously providing a microenvironment wherefrom the rapid uptake of the nutrients across the cell wall (Section 4.2.2) maintains a yet more dilute than the exterior environment and a helpful inward gradient. No compelling demonstration of this nutrient scavenging has been offered. For cells producing phosphatases designed to work externally (Sec- tion 4.3.3), there is a need to confine the activity close to the sites of intracellular uptake, which function could arguably be fulfilled by a mucilaginous boundary layer. To be valid, however, the entry of organic solutes must be faster than the loss of phosphatase. Again, no compelling experimental evidence is available to verify this.

Metabolic self-regulation Nutrient-deficient cells may be prevented from completing their division cycle (Vaulot, 1995) (see Section 5.2.1)but they cannot stop photosynthesis. Margalef (1997) proposed that sheaths slow down diffusion and minimise unnecessary metabolic activity. Although this idea fits with some of the field observations and also matches to the one well known to algal culturalists, that mucilage is usually lost CONSUMPTION BY HERBIVORES 273

quickly in laboratory strains, it is not clear that colonial species (e.g. of Coenochloris: Reynolds et al., 1983b) fail to attain maximum rates of growth under favourable supplies of nutrients and light. This they do without apparent loss or dimnution of the colonial form.

Defence against oxygen Sirenko and her co-workers (reviewed in Sirenko, 1972) demonstrated a low- redox microenvironment is maintained within the mucilage of several species of Cyanobacteria, apparently through the production of sulphydryl radicals. They have argued that this helps to protect against oxidative processes and leads to tolerance of high external concentrations of oxygen (similar comments were also made by Gusev, 1962, and Sirenko et al., 1969).

Defence against metal poisoning The selective permeability of mucilaginous envelopes might provide a defence against the uptake of toxic cations in the acidic environments tolerated by some desmids (Coesel, 1994). This idea has been investigated by Freire-Nordi et al. (1998), applying electron paramagnetic resonance to compare the decay rates of hydrophobically labelled tracers in normal sheathed cells of Spondylosium and in cells divested of their mucilage by ultrasound. Decay was slower in cells with mucilage, because of a suspected interaction with –OH groups in the polysaccharide. They concluded that such interactions could play a decisive role in uptake selectivity.

Defence against grazing Mucilaginous sheaths reduce the palatability of algae by making them too large for microplankters to ingest, more difficult for mesoplanktic raptors to grasp and less filterable and more mechanically obstructive for cladocerans (see Sections 6.4.2, 6.4.3). There is also recent evidence that free-living picocyanobacteria are stimulated to form colonial structures in response to the presence of herbivores and to the chemicals in the water that herbivores have recently vacated (Komárková and Simek,ˇ 2003) (see Section 6.4.2).

Defence against digestion If mucilaginous algae fail to avoid ingestion, they may resist digestion during the period of their passage through the guts of some (but not all) consumers. The original observations of Porter (1976)have been veriﬁed by others, including Canter-Lund and Lund (1995). The simultaneous scavenging of nutrients by viable algae during passage and their deployment is a bonus function of mucilage (see Section 6.4.2).

What may be concluded? There is no single clear function of mucilage, and not all those suggested could be considered valued judgements. The buoyant properties, the reducing microenvironment, the selective permeability and the grazing deterrence are backed by good empirical, experimental veriﬁcation. These may all be different, positively selected adaptations to what may have been originally homeostatic mechanisms for balancing cell stoichiometry. 274 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

concentration of 0.8 µgCmL−1 is necessary to sat- (Asterionella and, especially, Cryptomonas, Ankyra). urate its maximum assimilation. The correspond- With maturing individuals producing abundant ing minimal and saturating concentrations for parthenogenetic eggs and more animals recruit- the 2.1-mm adult are quite similar, at 0.14 and ing freely to the standing stock, the aggregate 0.87 µgCmL−1. daily filtration quickly appreciated to some 600- − − The figures make no allowance for wastage or -800 mL L 1 d 1 (Thompson et al., 1982;see rejection (Fig. 6.6)orfor the slightly different out- also top frame of Fig. 6.8). During this particu- comes at higher temperatures. A further aspect lar phase, the mean body length of a cohort of that was appreciated by Lampert (1977c)and individuals, feeding mainly on growing Ankyra ◦ developed by Lampert and Schober (1980)andGli- cells and at water temperatures close to 20 C, wicz (1990)isthat, for any filter-feeder, there is increased from 0.8 to 1.7 mm in 13 days and, an approximate upper threshold concentration simultaneously, recruited a fivefold increase of of edible, filterable foods when the maximum neonates of the next generation. Applying the physiological demands of growth and reproduc- contemporaneous direct estimates of Thompson tion are satisfied. This corresponds to the inflec- et al. (1982)toEq.6.14,therewas, over the same tion point shown in Fig. 6.4.Ofrathergreater period, a 12-fold increase in the collective filtra- significance, however, is the threshold food con- tion volume, Fi.Reynolds (1984a)usedthese centration that must be surpassed before an indi- measurements to express the resource-replete vidual animal can balance respiration and main- growth in Daphnia filtration as an exponent: from tenance and at which growth is zero. A slightly (ln 12) / 13 days, the specific rate of increase in Fi − ◦ higher threshold than this is necessary to main- is 0.1911 d 1 at ∼20 C. In contrast, recruitment tain the population, allowing some maturation of Daphnia had been negligible in April, when ◦ and egg production to offset mortalities (Lampert watertemperatures were still below 8 C, despite and Schober, 1980). an apparent abundance of food at that time (Fig. − To quantify the dynamic variability in the 6.8,toppanel: over 2 µgCmL1). Supposing relationship between food and feeders was a ageometric scaling of temperature dependence major objective of the studies in the Blelham of growth and recruitment capacity between 8 ◦ enclosures (Section 5.5.1,Fig.5.11). In the early and 20 C, Reynolds (1984a)approximated a rate part of the programme to measure loss rates of increase in the resource-saturated maximum − of primary product (Reynolds et al., 1982a), phy- aggregate filtration of 0.0159 K 1. toplankton was allowed to develop freeofthe The rate of change in the aggregate filtration constraint of nutrient supplies and the herbi- capacity (F)isnotthesamething as the popula- vore populations developed in an environment tion growth rate for Daphnia,although there are that was substantially free of predators. The analogies and some shared information. Growth deep-water enclosures (A, B in Fig. 5.11)were rates of Daphnia spp. under comparable condi- − devoid of any significant numbers of fish, while, tions noted in Gliwicz (2003a: ∼0.2 d 1)areof fortuitously, the restriction of enclosure open- similar magnitude. However, the seasonal fluc- ing tojustafewweeksinwinterprevented tuations in Fi provide a ready and reasonably theinward migration of chaoborid larvae from sensitive indicator of the impact of grazing on their shallow overwintering sites (Smyly, 1976). thefood resources and the consequences of food Thus, it has been assumed that the herbivore depletion on the survival of Daphnia.Ofthe periodicities that were observed were susbstan- examples from the Blelham enclosures plotted tially driven from the bottom up, being regulated in Fig. 6.8,reference has already been made to mainly by temperature and variable food avail- events in Enclosure A during 1978 (A78). Sub- ability. An example is included in Fig. 6.7.Once ject to satisfaction of the temperature constraint, ◦ watertemperatures exceeded 7--8 C, daphniids theepisodes of increase in Fi (at one point, to − − rapidly established themselves as the most signif- >1LL 1 d 1)wereobserved in the presence of a icant consumers, responding quickly to an abun- finite resource base of filterable algae (defined in dance of algae of filterable size food resources thestudy as being individually <104 µm3;mean CONSUMPTION BY HERBIVORES 275

Figure 6.7 Seasonal variations in the abundances of the main zooplanktic species in the Blelham Enclosure A, during 1978. The numbers of Daphnia in each of ﬁve size categories are shown separately (I, < 1.0 mm, 17 ± 3 ◦C; II, 1.0− 1.3 mm; III, 1.3−1.6 mm; IV, 1.6− 1.9 mm; V, > 1.9 mm). Redrawn from Reynolds (1984a).

d = 26 µm). These increases were not sustained, response of the aggregate filtration rate could however, as the calculated aggregate filtration scarcely be better correlated. capacity periodically collapsed, owing, on each Overall, there is manifestly no reciprocity occasion, to severe reductions in the numbers between food and feeders, whereas, under of filter-feeders present. In almost all of these the contrived conditions, the latter plainly instances, the herbivore collapses followed severe tracked the former. Baldly, without a resource, depletion in the filterable algal mass. In Enclo- filter-feeding is unsustainable. Filter-feeders can sure B in 1979 (B79), aggregate filtration rate was increase, provided the minimum threshold con- generally reduced and confined to a narrower centration of edible, filterable foods is exceeded. time window than in A78, owing to the dom- The evidence from Fig. 6.8 is that the threshold inance of the algal biomass by Planktothrix (in is pitched between 0.10 and 0.13 µgCmL−1. Sub- spring) and Microcystis (in summer). Both were stantially greater concentrations than this will considered to be inaccessible food resources to support growth of filter-feeders. Once the aggre- the filter-feeders on the grounds of size. In B81, gate rate of loss of algal foods to filter-feeders grazing was generally modest throughout a year (rG)isinexcess of the net rate of their recruit- when filterable foods were conspicuously low ment (r ,orr net of all other simultaneous loss throughout the year. In A83, filterable foods were rates), rapid exhaustion of the food resource (to abundant in the spring but not in summer; the <0.10 µgCmL−1)isinevitable. This is followed, 276 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.8 Seasonal variations in the phytoplankton biomass (as carbon) in Blelham enclosures during selected years and its approximate fractionation between filterable (hatched) and non-filterable (unshaded) size categories. The bold dashed line is the aggregate daily filtration rate generated by the zooplankton, which, at times, exceeded 1.0 (sensu 1 litre per litre of enclosed water volume per day). Note that the filtration volume mainly reflects the numbers of filter feeders present and that it responds to the availability of suitable foods (abundance and filterability). Redrawn with permission from Reynolds (1986b).

almost as inevitably, by starvation and death, par- 16.5 s. At food concentrations below this thresh- ticularly of the neonates (Ferguson et al., 1982). old level, animals of both sizes will fail to ingest sufficient food to satisfy their minimum needs. Food thresholds and natural populations In reality, several potential foods may be present For completeness, the lower and upper thresh- but, if their combined carbon content (supposing old concentrations impinging on the ability of D. it to be wholly filterable and assimilable) is sub- galeata populations to survive or to saturate their stantially below the threshold concentration, the capacity for growth are expressed in terms of the animals will starve. populations of some common fresh-water plank- While it is proposed that these thresholds ters (Table 6.3). The concentrations cited should set firm boundaries within which the mutual be interpreted as defining the fufillment or sat- dynamics of phytoplankton and zooplankton uration or otherwise of the Daphnia’s nutritional interact, it is also fair to say that, in the real requirements, were the food resource monospe- world, they are not often easily recognisable. cific. For example, were Cryptomonas ovata the There are several reasons for this and they need only food available, a population of 175 mL−1 to be acknowledged. First, not all filter-feeding would be the minimum that will could meet the zooplankton need experience the same threshold feeder’s basic maintenance needs at 15 ◦C. In the concentrations. Second, there is the subsidiary case of the 0.8-mm neonate, filtering up to 5 mL issue that larger individuals of any filter-feeding of water during each 24 h, it would be expected species can ingest larger prey. This means that to encounter 875 algal cells in a day, at an average thelower metabolic threshold can be fulfilled by frequency of one every 99 s. A 2.1-mm adult, feed- awider size range of foods, so that the resource ing in the same suspension, should be capable of base of the larger filter-feeder is greater than ingesting 5250 algae during the day, or one every that of the smaller one. Moreover, the algal food CONSUMPTION BY HERBIVORES 277

Ta b l e 6.3 Equivalent concentrations of selected algal and bacterial foods representing the minimum and saturating threshold requirements of Daphnia maintenance, growth and reproduction

Populations equivalent to Volume Cell C Food species (µm3) (pg) 0.1 µgCmL−1 0.8 µgCmL−1 Cryptomonas ovata cell 2710 569 175 1 406 Scenedesmus quadricauda 1000 225 444 3 560 (four-cell coenobium) Asterionella formosa cell 645 85 1 176 9 411 Plagioselmis nannoplanctica cell 72 15 6 667 53 333 Synechococcus cell <30 <7 >14 285 >114 280 Ankyra judayi cell 24 5 20 000 160 000 Free-living bacteria – 0.013 7.7 × 106 6.2 × 107

resource of all filter-feeders may be supplemented imum threshold is some 4--7 × 106 mL−1.Evenin to a degree byaresource of suitably sized partic- these instances, any further inroad into the fil- ulate organic matter (detritus) and by free-living terable resource leaves filter-feeders severely food bacteria. Finally, predation of planktic herbivores limited. Almost all the other components of the distorts the impression of community structure, microbial food web, including the nanoflagellates function and the outcome of dynamic processes. and ciliates, as well as fine, suspended detritus, Gliwicz (1990) compared the body-growth will have been eliminated by daphniids feeding rates ofanumberofDaphnia and Ceriodaphnia in significant numbers (Porter et al., 1979;Jurgens¨ species as a function of food concentration. Some et al., 1994; Sanders et al., 1994;Wiackowski et al., modest interspecific differences in the lower 1994). thresholds were evident (in certain cases, these Do these thresholds not then determine that − could be as low as 0.03 µgCmL1), with the theabundance of zooplankton in pelagic systems best survivorship being noted among the larger having a biological supportive capacity substan- species of D. magna and D. pulicaria.Giventhat tially greater than 0.1 mg C L−1 would tend to larger animals also filter more water and ingest alternate between glut and self-inflicted dearth larger particles, we may deduce that, potentially, of the largest filter-feeding species present? In adults of the larger species, together with mature the case of Blelham Enclosure A in 1978 pre- adults of the intermediate size classes, enjoy a sented above, the surges and collapses in the wider filterable resource base and may be better Daphnia population would appear to conform to adapted to survive instances of periodic starva- this supposition. Elsewhere, of course, the zoo- tion than juveniles or adults of small species. plankton dynamics are moderated by planktivory On balance, ecological evidence is supportive (and especially by fish) which tends to damp of the physiological deduction. Daphniids of all the fluctuations between famine and plenty. kinds seem to be relatively scarce in the plankton Furthermore, the zooplankters that are both of lakes in which the carbon supportive capac- more visible and more rewarding to the plank- − ity isgenerally ∼0.1 mg C L 1. Moreover, devel- tivore are the larger ones, and, other things opment in waters where the supportive capacity being equal (see Sections, 6.4.5, 8.2.2, when inter- may only coincide with filterable POC concentra- actions and entire pelagic resources are dis- − tions >0.05--0.1 mg C L 1.Iffulfilled exclusively cussed), selection is against large animals and in by algal plankton, the corresponding threshold favour of the survival of smaller animals and of is equivalent to a chlorophyll concentration of 1- smaller species that reproduce at smaller body − -2 µgchla L 1.Ifsubstituted by bacteria, the min- sizes (Gliwicz, 2003a, b). As a consequence, the 278 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

survival prospects of each species in the zoo- tive and the effects of filter-feeding zooplankton plankton and the resultant structure of the com- on phytoplankton are less intensively regulated munity are poised between the influences of food than they are above it. limitation and herbivore predation. Zooplankton The elegant study of the feeding selectivity ecologists have, for long, recognised the interac- of young roach (Rutilus rutilus)undertaken by tion between, on the one hand, the ability to Townsend et al. (1986)revealedtheprogressive feed, assimilate, grow and reproduce under con- switching between benthivory and planktivory ditions of resource stress and, on the other, the in response to the abundance of planktic crus- vulnerability to predation. The balance of these taceans in the range 10--50 mg C L−1. The implied counteracting influences was expressed in the threshold is not a fixed one, for it depends upon elegant size-efficiency hypothesis (SEH) of Brooks the availability and accessibility of benthos, as and Dodson (1965). Planktivory intervenes in the well as upon the numbers of fish competing for tendency of the large-bodied species of zooplank- it. Its existence explains tacit upper limits on ton tomonopolise the resources to the exclusion the concentrations of filter-feeding zooplankton of small-bodied species (including, it might be (equivalent to as few as 10--20 large Daphnia L−1 added, those of the microzooplankton). Selective but 100--200 small-bodied species: Kasprzak et al., predation of large-bodied species favours larger 1999), that could be set as much by their attrac- populations of small-bodied species that repro- tivity to predators as by the sustainability of their duce when they are still small. The relative abun- phytoplanktic food resources. The consequences dance of large- and small-bodied species is thus impinge on the structure of planktic food webs, strongly influenced by the intensity of predation thepredominant energy pathways in aquatic sys- by planktivores (cf. Hrba´ˇcek et al., 1961). tems and the role of the phytoplankton in sus- Although the broad thrust of the SEH remains taining either. These issues are the subject of wholly acceptable, it is important to recog- Section 8.2. nise Gliwicz’s (2003b)distinction between the dynamic effects of the immediacy of predation 6.4.3 Selective feeding and the gradual debilitation forced by food short- In fresh waters, mesoplanktic filter-feeding ages. The relationship is further complicated by clearly has a lower threshold of viability, that thefact that, in shallow or marginal areas of falls in the range 0.03--0.1 µg filterable C mL−1 water bodies, predators may easily switch their (30--100 mg C m−3). This value is set by the biol- foraging efforts to the frequently more rewarding ogy of the most successful cladocerans and not resources of the littoral and sub-littoral benthos. by some physiological override. After all, tuni- In this way, the intensity of planktivory on sparse cates survive in oceanic waters supporting chloro- zooplankton populations may be less than might phyll concentrations habitually in the range 0.1-- be deduced from the abundance of predatory 0.3 µgchla L−1 (say, 5--15 mg C m−3). In fairness, species. Thus, it may be only in the true pelagic, it must be added that the filtering rate to body well away from the influences of shores and sedi- mass in tunicates has to be high and their rates of ments, that planktivory exerts the expected con- growth are modest compared with those of clado- tinuous constraint on the growth and recruit- cerans (Sommer and Stibor, 2002). The only viable ment pattern in the zooplankton. Elsewhere, the foraging alternative in the rarefied, low-biomass effects of planktivory on the zooplankton may be worlds of the open pelagic, of both marine and amorecasual or more opportune constraint, at fresh-waters, is to be able to locate and select prey least until the zooplankton offers a sufficiently of high nutritive value and to be successful in its abundant and attractive alternative food refuge. capture. The corollary of this deduction is that there is The point has been made above that this abil- a further conditional threshold for the feeding ity is particularly developed among the plank- pressure exerted on the phytoplankton that is tic copepods. The majority of cyclopoids are dependent upon herbivore engagement. Below it, exclusively raptorial, feeding on algae in their thebenthic alternatives remain the more attrac- juvenile naupliar stages, then becoming more CONSUMPTION BY HERBIVORES 279 carnivorous in the later copepodite and adult There is thus considerable complementarity stages, when they actively select rotifers and in the respective dynamics, spatial and tem- small cladocerans. Adult calanoids have the abil- poral distributions of calanoids and daphniids. ity to filter-feed but they have the further facility Though they frequently coexist in mesotrophic to supplement the spectrum of available foods by and mildly eutrophic lakes, the obligately filter- seizing, grappling and fragmenting microplank- feeding cladocerans are unable to satisfy their tic algae. When both options are available, adult metabolic needs at chronically low food con- diaptomids supplement the yield of filter-feeding centrations. Thus, calanoid dominance is rela- with larger items that they capture, and usu- tively common among oligotrophic lakes, usually ingest more food than could have been sup- ally in association with an underpinning micro- plied contemporarily through filter-feeding alone bial food web. If the supportive capacity of (Friedman, 1980). The benefit of doing so presum- POC (be it detrital, bacterial or algal) is signif- ably increases inversely to deficiency in the con- icantly >0.1 mg C L−1, Daphnia should be able centration of nanoplanktic particles available. to thrive and, for so long as the food concen- Moreover, upward extension of the size range of tration satisfies the demand, to reproduce and ingestible foods to 30 µmormore permits adults recruit new individuals rapidly. The condition of Eudiaptomus to feed on algae as large as Cos- may persist until, potentially, the Daphnia popu- marium and Stephanodiscus (Gliwicz, 1977;Rich- lation is processing such large volumes of water man et al., 1980). However, it is the selection of each day that not just the recruitment of detri- ciliates (e.g. Strickler and Twombley, 1975;Hart- tus, bacteria and filterable algae but also the com- mann et al., 1993)that most broadens the main ponents of the entire microbial food web are diet of calanoids. This may be critical to their sur- exhausted (Lampert, 1987;Weisse, 1994). Other vival in very oligotrophic marine and fresh-water things being equal, such occurrences are fol- systems, wherein it also proves to be the deci- lowed by significant mortalities of cladocerans sive trophic linkage in the carbon metabolism of and, to a lesser extent, other mesozooplank- lakes and seas of low biomass-supporting capac- ters too (Ferguson et al., 1982). These observa- ity (Cole et al., 1989;Weisse, 2003)(seealso tions fit well with established features of lim- Section 8.2). netic zooplankton ecology, especially those relat- The undoubted effectiveness of calanoid for- ing to shifts in dominance. Cladocerans gener- aging under these circumstances combines the ally respond positively to anthropogenic eutroph- animals’ well-developed ability to select the sizes ication (Hillbricht-Ilkowska et al., 1979), bringing of food attacked and ingested with their impres- greater amplitude of fluctuations in the biomass sive facility to be able to chemolocate (De Mott, of Daphnia and its foods (McCauley et al., 1999; 1986), then orientate towards and strike out at Saunders et al., 1999). their potential prey organisms (Strickler, 1977; Notall cladoceran families are obligate filter- Alcaraz et al., 1980;Friedman, 1980). The abil- feeders. Some of the littoral-dwelling chydorids ity of calanoids to survive on modest rations and macrothricids have thoracic limbs that are is a further factor contributing to their fre- adapted to scrape periphyton from the surface quent dominance of the oligotrophic mesozoo- of leaves, etc. Chydorus sphaericus is frequently plankton (Sterner, 1989). To judge from Hart’s seen among larger microphytoplankton in small, (1996) data (see P. 262), calanoids are able to eutrophic lakes, often clutching onto colonies draw sufficient food to satisfy their maintenance such as Microcystis and scraping epiphytes from demands from POC concentrations that are an the mucilage (Ferguson et al., 1982;Ventela¨ et al., order of magnitude more dilute than those tol- 2002). Though the bosminids have filtering phyl- erated by cladocerans. Their demands for energy lopods and use them for this purpose for much of and reproductive investment may well be satu- thetime, they are also capable of supplementing ratedatfood concentrations (0.08 µgCmL−1)that nanoplanktic particles from the water by seizing would hardly keep Daphnia from slowly starving larger individual prey items. To do this, they to death. use the (fixed) antennules, abdominal claw and 280 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

carapace gape, fragmenting the potential food of between 0.1 and 0.2 µgC(µgC)−1 d−1. to pieces of more ingestible size (De Mott, 1982; The imposition of selective herbivory on the Bleiwas and Stokes, 1985). Selectivity of food is relevant size ranges of speciﬁc foods may be aided by chemoreception (De Mott and Kerfoot, approximated from the sum of the individual 1982). number--mass products of consumers per unit Neither are the advantages of food selectivity volume. Byanalogy to Eq. (6.13), conﬁned to the exploitation of scarce resources G = (N · G ) + (N · G ) +···(N · G ) (6.15) in oligotrophic conditions. In waters rendered 1 1 2 2 i i

turbid through the repeated resuspension of where Gi is the ingestion rate and Ni is the stand- clay and fine silt particles (1--20 µm), asmany ing population of the ith species-size category of or more of the food-sized particles are inert and selective grazer. Finally, a rate of grazing on the near useless and greatly diminish the benefits of food species affected, to be set against other expo- filter-feeding. Selective feeding provides a more nents of change for the food species affected. productive food return for the foraging effort. r = (G )/V (6.16) This is a functional explanation for the common G observation that the zooplankton of turbid By way ofanexample,Ferguson et al. (1982) lakes, even quite eutrophic ones, is typically observed populations of Eudiaptomus gracilis in dominated by calanoids or small cladocerans planktivore-free enclosures of up to 20 adults (Allanson and Hart, 1979;Arruda et al., 1983). L−1. Supposing an average length of 1.5 mm High densities of large or mucilaginous algae in and an individual mass equivalent to 9.3 µgC, productive waters also constitute a nuisance to food intake may be approximated to be <2 µg large, obligate filter-feeders such as Daphnia,espe- Canimal−1 d−1, with the population demand cially when the algae are close to the upper limit- peaking at <40 µgCL−1 d−1.Intermsof the ing size. Although Daphnia species exercise their principal food ingested at that time, Asterionella limited powers of food selection (varying the (85 pg C cell−1), the maximum demand could carapace gape), they do less well than bosminids have been equivalent to a loss of not more than that filter-feed on abundant nanoplankton and 470 cells mL−1 d−1.For smaller populations of bacteria nourished by organic solutes released smaller animals at lower temperatures, the food from the algae. Cascading reactions among the demand would normally have been rather lower heterotrophic nanoflagellates are also noted than this maximum (perhaps 10--20 µgCL−1 (Ventela¨ et al., 2002). An analogy comes to mind d−1 is a more likely optimum). Numbers may of small animals grazing or browsing among be sustainable on the relatively smaller daily trees, which are, nevertheless, of sufficient size rations of just 1--2 µgCL−1 d−1.Relative to algal and density to exclude larger animals. In the standing crops, the removal of 470 cells mL−1 end, these same larger algae may share part of d−1 is scarcely sustainable by anything under the role ofplanktivorous fish in defending the 500 cells mL−1 doubling each day but, to a entire community against total elimination by standing crop of 10,000 cells mL−1,itrepresents −1 overwhelming Daphnia filtration rates. an exponential loss rate of rG < 0.05 d . The demand made on the resources by selective feeders is more difficult to gauge than is 6.4.4 Losses to grazers that of less specialised filter-feeding. The carbon The combined effects of selection and filter- intake required by calanoids saturates at close feeding impose differential rates of removal upon to the minimum requirements of filter-feeding thespecies composition of the phytoplankton. cladocerans. In consideration of a small (0.8-mm) Some (mostly smaller species, generally <50 µm and large (2.1-mm) Daphnia,thesupposed mini- in maximum dimension, but often mainly mum daily carbon requirements (0.6 and 4.3 µg nanoplanktic species) are removed primarily by Crespectively) service projected body masses cladoceran filter-feeding but also by other crus- equivalent to 3.2 and 42 of µgCrespectively taceans. Others, generally the smaller microphy- (Box 6.2), to provide daily carbon-specific intakes toplankters (20--100 µminmaximum dimension), CONSUMPTION BY HERBIVORES 281

Box 6.2 Carbon equivalents of planktic components

In interrelating observations on the biomass and production of plankton with the distribution and ﬂow of organic carbon through pelagic ecosystems, it is helpful to have a ready base for interconversion. Many such conversions are available in the literature and some have been invoked in this book. The selection of conversions below is the one used throughout this book. The veracity of the relationships is not always well known and, for any particular species, something better can generally be found. On the other hand, for generalisations and order-of-magnitude ﬂux estimates, the following statements will be found to be helpful.

Free-living bacteria Conversions linking carbon content and biovolume were explored by Lee and Fuhrman (1987); more general averages (0.01–0.02 pg C cell−1) are given in Sorokin (1999). In calculations here, I follow the determination adopted by Ferguson et al. (1982)for freshwater bacteria in a eutrophic reservoir: 1 × 106 cells / 13 ng , or carbon content of bacteria, 0.013 pg C (cell)−1.

Non-diatomaceous phytoplankton As developed in Section 1.5 the carbon content of most phytoplankters (save for diatoms) conforms well to the regression C = 0.225 v0.99 (Fig. 1.8) where v is the cell volume. Thus, the carbon content of planktic algae is ∼0.225 pg C µm-3. (Individual cells range from >1pgto10ngC.)

Diatoms The large vacuole and high ash content of the cell wall make it difﬁcult to rely on the above relation. A more reasonable estimate is to take C = 50% of the ash- free dry mass. The ash content can be approximated on the basis of cell volume according to the regression in Fig. 1.9.Table 1.5 suggests an average Si of 0.1 pg Si (or 0.21 pg ash) per µm3 of cell volume. In this case, 0.15pg C µm−3 is also a helpful approximation.

Nanoﬂagellates Assumed to conform to the relationship for phytoplankton. Thus, carbon content of planktic algae is ∼0.225 pg C µm−3 (individual cells in range 1–900 pg C).

Ciliates Pending better information, individual cells probably range from 1 to 100 ng. Herein, ‘small planktic ciliates’ are considered <30 µm, with a carbon content of ∼3pgC; ‘large ciliates’ (60 µm) may easily comprise 50 ng C. 282 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Rotifers Examples from Bottrell et al. (1976), assuming carbon is 50% dry weight. All means subject to margin of at least ±30%. Polyarthra spp. 35 ng C (individual)−1 Keratella cochlearis 50 ng C (individual)−1 Kellicottia longispina 100 ng C (individual)−1 Brachionus calyciﬂorus 110 ng C (individual)−1 Filinia longiseta 150 ng C (individual)−1 Keratella quadrata 150 ng C (individual)−1 Asplanchna priodonta 250 ng C (individual)−1 Cladocera: Daphnia Bottrell et al. (1976) collected, presented and pooled a wide range of regressions

relating body mass to body length in Daphnia,ofthe form ln (Wanimal) = ln a + b

ln (Lanimal). With Lb in mm, W (in µg) is generally well predicted by the slope b = 2.67 and the intercept ln a = 2.45. Subtraction of ln 2 (0.693) gives the prediction

ln[C ] = 2.45 − 0.693 + 2.67 ln(L b). Some examples: −1 Lb = C (individual) = 0.8 mm 3.2 µgC 0.95 mm 5.0 µgC 1.3 mm 11.7 µgC 1.6 mm 20.3 µgC 2.1 mm 42 µgC 2.24 mm 50 µgC 4.0 mm 234 µgC Cladocera: Bosmina Bottrell et al. (1976) pooled several regressions relating body mass to body length

in Bosmina,oftheform ln (Wanimal) = ln a + b ln (Lb). With Lb in mm, W (in µg) is generally well predicted by the slope b = 3.04 and the intercept ln a = 3.09. Subtraction of ln 2 (0.693) gives the prediction

ln[C ] = 3.09 − 0.693 + 3.04 ln(L b). Some examples: L = C (individual)−1 = 0.3 mm 0.3 µgC 0.7 mm 3.7 µgC 1.0 mm 11.0 µgC Copepoda Bottrell et al. (1976) pooled several regressions relating body mass of copepods

to body length of the form ln (Wanimal) = ln a + b ln (Lb). With Lb in mm, W (in µg) is generally well predicted by the slope b = 2.40 and the intercept ln a = 1.95. Subtraction of ln 2 (0.693) gives the prediction

ln[C ] = 1.95 − 0.693 + 2.4 ln(L b). CONSUMPTION BY HERBIVORES 283

Some examples: −1 Lb = C (individual) = 0.1 mm 0.014 µgC 0.3 mm 0.2 µgC 1.0 mm 3.7 µgC 1.5 mm 9.3 µgC 2.0 mm 18.5 µgC 2.5 mm 31.7 µgC Satapoomin (1999) published relationships of mass and carbon content for several marine species of copepods. For body lengths of 0.5 to 1.4 mm, Centropages carbon contents of 0.5–16.6 µgC(individual)−1 and Temora 1–33 µgC(individual)−1 are found.

Euphausiids Lindley et al. (1999) presented regressions relating body mass of some euphausians

to various allometric length measures, in the form log (Wanimal) = a + b log (Lc),

where Lc is the body length from the rostrum to the telson tip. Putting a = 0.508 and b = 2.723, and the typical carbon content of 40% dry mass, [C] is predicted as:

ln[C ] = 0.508 − 0.4 + 2.723 log(L c). Some examples: −1 Lc = C (individual) = 2mm 8.5 µgC 6.3 mm 193 µgC 20 mm 13 620 µgC

are taken mainly by calanoids. Larger micro- feeding is normally capable of clearing the water plankton may be immune from either, although of small algae and can almost wholly account for even these may be liable to specialist predators, the demise of extant populations. which may include rotifers and protists. Because it still seems to generate surprise In the size range, 20--50 µm, phytoplankton among some limnology students, it needs to be may beliabletoattack by both main kinds of emphasised again that the simultaneous pres- crustacean. The dynamic rates of their removal ence of grazers and grazed species is in no way from their respective populations should be for- incompatible. In fact, with the one being depen- mally restated by combining Eqs. (6.14)and dent upon the other, no other possibility is ten- (6.16): able. Referring back to Eqs. (5.3)and(6.1), grazing is tolerated by the grazed population so long > as r rL and rn remains positive. True, the rG = [ω (F i) + (G )]/V (6.17) rate of loss, rL,atleastforsomespecies,maybe very largely attributable to the rate of removal In relative terms, selective feeding is the more by grazers, rG. Moreover, rising removal rates, prevalent loss process where filter-feeders fail especially from recruiting populations of clado- to operate. However, as has been suggested, the cerans, can easily exceed declining rates of algal dynamic effect of filter-feeding, where itissustain- recruitment. These are the circumstances of the able,ispotentially much greater than selective rapid elimination of the food species. Certainly, feeding in absolute terms. Only cladoceran filter- under these conditions, loss to grazers becomes 284 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Ta b l e 6.4 Derived rate constants for two consecutive development phases of the nanoplanktic alga Ankyra judayi in Blelham Enclosure A during the summer of 1978

a b Period Observed rn rS rG Back-calculated r 12 Jun–3 Jul 0.497 0–0.143 0.193–0.622 0.690–1.262 3 Jul–10 Jul 0.122 c 0.644–1.416 >0.766 10 Jul–24 Jul −1.043 0–0.082 0.595–1.341 0–0.380 14 Aug–28 Aug 0.493 0–0.344 0.418–2.022 0.911–2.859 28 Aug–4 Sep −0.150 0.046–0.068 0.253–0.556 0.149–0.474 4 Sep–18 Sep −0.643 0 0.244–0.714 0–0.071

a Estimated from sediment traps set at depth. b Calculated from aggregate ﬁltration rate only, assuming no rejection (ω = 1). c No traps set.

the main fate of the phytoplankton population in The upper sinking loss rates predict a bulk sedi- question. mentation rather greater than was actually mea- In mesotrophic and in mildly eutrophic lakes, sured during the same experiments (Reynolds grazing losses are evidently heavy among species and Wiseman, 1982). Thus, the additions to the vulnerable to filter-feeding. Reynolds et al. (1982b) one precise statistic, the observed net rate of commented on the poverty of nanoplankton and increase, rn, should err on the low side. small microplankton that were recoverable in The exponents are used to back-calculate the deep sediment traps in Windermere. In the much bulk additions or subtractions in each phase. shorter water columns of the experimental lim- Thus, supposing netic enclosures in Blelham Tarn, too, abundant N = N exp (r − r − r )t (6.18) growths of Cryptomanas, Plagioselmis, Chromulina t 0 S G and, especially, Ankyra that, at various times, then the increment or decrement is given by: were stimulated (Reynolds, 1986b) contributed lit- − = { − − − } tle to the sedimentary flux. Within the confines Nt N0 N0 [exp (r rS rG)t] 1 (6.19) of the enclosures, some reasonable approxima- whence the number of cells produced (P)iscal- tions of the rates of grazing removal were possi- culated as ble. The entries in Table 6.4 track the changes in = / − − { − − − } therates of increase and decrease through two P [r (r rS rG)] N0 [exp (r rS rG)t] 1 consecutive peaks of Ankyra in Enclosure A in (6.20) 1978 (during which weekly fertilising averted the By analogy, the number of cells sedimented (S) likelihood of nutrient limitation and the main and grazed (G)arecalculated: grazers, Daphnia galeata,werealmostuncon- = / − − { − − − } strained by predators). The estimates necessar- S [rS (r rS rG)] N0 [exp (r rS rG)t] 1 ily carry large error margins: these are properly (6.21) shown, although it may be confidently stated that G = [rG/(r − rS − rG)] N0{[exp (r − rS − rG)t] − 1} the lower ends of the ranges shown are more real- (6.22) istic in each case. The true rate of replication (r ) of Ankyra under the general conditions of light In either of the depicted instances, Ankyra cells and temperature obtaining during these times were first detected in near-surface water at con- could scarcely have much exceeded 1.0--1.1 d−1 centrations in the order of 20--40 cells mL−1. in the earlier phase whereas a rate between 0.9 In July, this built to a maximum of over and 1.0 would have applied during the second. 300, 000 cells mL−1,still mainly confined to the CONSUMPTION BY HERBIVORES 285

Ta b l e 6.5 Calculated production (P)ofAnkyra cells and losses attributable to sedimentation (S) and grazing (G)in each of the periods noted in Table 6.4

Period P (cells m−2 × 10−9) S (cells m−2 × 10−9) G (cells m−2 × 10−9) 12 Jun–3 Jul 905–1655 0–188 253–816 3 Jul–10 Jul 5520–11084 c 4641–10204 10 Jul–24 Jul 0–556 0–120 871–1962 a 6425–13295 0–308 5765–12982 RW82b <14

14 Aug–28 Aug 1466–4601 0–554 673–3255 28 Aug–4 Sep 513–1631 158–234 871–1914 4 Sep–18 Sep 0–31 0 106–309 a 1979–6263 158–788 1650–5478 RW82 4–5

a is the total over the wax and wane period. b RW82 is the direct measurement of Reynolds and Wiseman (1982)over the whole population. epilimnion (1531 × 109 m−2). The contempora- zooplankton interactions. It is generally true that neous development of a Daphnia population (see neither functions independently of the presence Fig. 6.7)was shown by gut-content analysis to of the other, even if there is no direct link- be largely sustained on Ankyra (Ferguson et al., age between the components. Excepting large 1982). Solution of Eq. (6.22)indicates that not colonial phytoplankters (like Microcystis or Volvox) fewer than 4891 × 109 Ankyra cells m−2 would whose consumers are more likely to be epiphytic have been eaten by then. Thus, not fewer than than planktic, or those microzooplankters whose 6422 × 109 cells m−2 would have been produced diet may be exclusively bacterial, most phyto- (for comparison, the potential production of cells plankton is liable to become the food of some over the sameperiod and at a sustained rate of zooplankton at some time. Removal of primary- 0.69 d−1 would have led to the production of 49 producer biomass as the food of herbivores × 1015 cells m−2!) By the end of the population, inevitably means that phytoplankton biomass is which was also rapidly cleared by grazers, losses smaller than it would have been had there been to Daphnia of >5765 × 109 cells m−2 accounted no grazing. The converse might be that there (Table 6.5)for 90% of the inferred production. would be a smaller consumer biomass if the con- In the second phase of Ankyra growth, which sumers were denied access to primary foods and built to a maximum of 671 × 109 cells m−2, that these were not supplemented by an energet- thededuced production was not less than 1979 ically equivalent organic carbon source. × 109 cells m−2,ofwhich> 1650 × 109 m−2 If that much ‘states the obvious’, it has to be would have been cropped by grazers, whereas said that there are few other popular assump- the directly measured sedimentary export was tions about the interactions between phytoplank- <5 ×109 m−2 (<0.3% of the total production). tonand zooplankton that are passed unchallenged. For instance, there is no clear reciprocity 6.4.5 Phytoplankton–zooplankton between the abundance of phytoplankton and interactions of zooplankton (see the examples in Fig. 6.8), In order to draw a general perspective on although there may be an element of the ‘track- the effects of consumers on the phytoplankton ing’ by zooplankton numbers of ﬂuctuations in and on the export of primary production to edible biomass. There is little evidence, either, theaquatic food webs, it is helpful to formu- that grazing by zooplankton necessarily con- late some overview of nature of phytoplankton-- trols the dynamics of the phytoplankton in any 286 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

also fittest to exploit opportunities. In this sense, either the best competitors (sensu Keddy, 2001)or the most exploitative animals will be favoured to succeed. This generalisation is well exemplified by thetwo major groups of herbivores -- calanoids and cladocerans -- in lake plankton. The daphniid cladocerans, especially, are efficient in gathering and concentrating uniformly small food particles from dense suspensions and, also, in then turning carbon resource into new daphniid biomass. Subject to the satisfaction of an overid- ing condition of food adequacy, daphniids are exploitative and expansive, and tend to dominate overwhelmingly all other zooplankters, if not by eating them, then by eating out their resources. Their sensitivities relate to these same adaptations: having the potential to grow to Figure 6.9 Season-long comparison between (a) the numbers of phytoplankton species attaining maximal large numbers and to relatively large individual population within a given week of the year and (b) the body sizes makes them disproportionately vul- contemporaneous zooplankton biomass. There is no nerable to planktivorous predators. Their restric- correlation, in spite of the fact that the phytoplankton tion to filterable foods leaves them vulnerable development was never nutrient-limited and the zooplankton to diminished and to chronically low concentra- was almost entirely unpredated. Data from Ferguson et al. tions of algae and, perhaps surprisingly, also to (1982)for Blelham Enclosure A 1978, and redrawn with an abundance of algae of varied or of larger sizes, permission from Reynolds (1987b). that interfere with systematic filtration of the resources. In stark contrast, the calanoid cope- predictable way. To judge from the example in pods fill in many of the gaps left by cladocerans Fig. 6.9,there is no correlation between the num- through superior economy on a small resource bers of phytoplankton species achieving their base and through greater discrimination in feed- respective population maxima and the biomass ing on large food particles. Analogous principles of unpredated herbivores. probably apply in the open sea, save that conditions of resource deficiency are more general Competitive interactions and more persistent. Cladoceran filter-feeding is Part of the complexity of these otherwise obvi- seen to bring smaller returns than are earned by ous relationships is due to a wide range of inter- calanoid selectivity. specific interactions between key consumers and The interactions between the abundance and keyprimary producers; another part is the conse- species structure of the phytoplankton and the quence of forcing by the consumption at higher zooplankton are similarly contrasted according trophic levels. There are also some effects trans- to whether the phytoplankton is cropped mainly mitted in the opposite direction, whereby phy- by calanoids or cladocerans. Using small enclos- toplankters benefit from the presence of zoo- ures (mesocosms) placed in a mesotrophic lake, plankters. Consideration reveals some interesting Sommer et al. (2001) observed the effects on discernable patterns in the linkages among the the composition of the summer phytoplank- main food organisms and the main groups of tonofexperimental adjustments to the relative feeders. Gathering sufficient food to support sur- abundances of Daphnia and Eudiaptomus. The sup- vival and reproduction is a general problem for pression of small phytoplankton by dominant most animals, while those that are most efficient Daphnia and the suppression of larger species in converting extra energy into extra biomass are by Eudiaptomus occurred much as predicted, CONSUMPTION BY HERBIVORES 287 although the authors noted that neither was able through bacteria and consumers. This might also to graze down the phytoplankton to the low con- apply to undigested foods rejected (but not nec- centrations frequently observed in cladoceran- essarily undamaged) by so-called ‘sloppy’ filter- dominated lakes in spring (Lampert, 1978; feeding. Cladocerans produce a rather diffuse Sommer et al., 1986) (see also Fig. 6.8). Yoshida and amorphous waste which seems more recy- et al. (2001)also undertook mesocosm experi- clable in the immediate vicinity of its release. It ments on an oligotrophic lake plankton, testing seems likely that, even then, bacterial mineralisa- theeffect of fertility and macrozooplankton on tion plays a large part in regenerating nutrients community structure. Raising the fertility alone that, once again, become available to phytoplank- led to a higher biomass of algae inthenano-and ton. Probably of greater importance are the quan- microplanktic size ranges and to more numerous tities of nitrogenous or phosphatic metabolites heterotrophic nanoflagellates. The response to that may be excreted across the body surfaces of higher populations of Eodiaptomus japonicus con- zooplankters. These are soluble and also readily formed to a cascading impact, with fewer ciliates bioavailable to algae (Peters, 1987). The restora- and bacteria but more heterotrophic nanoflagel- tion of nutrients to primary producers is one of lates. With Daphnia galeata,algae, nanoflagellates thewaysinwhich pelagic ecosystems contribute and microzooplankton were all suppressed. to their own self-regulation and maintain their With enrichment raised to the level of eutro- own resource base (e.g. Pahl-Wostl, 2003). phy, when nutrient availability can support high The excretory wastes will always be domi- levels of producer biomass, cladoceran feeding nated by the metabolites in excess. It has been may eventually select against smaller algae and pointed out (Hessen and Lyche, 1991; Elser et al., in favour of the larger forms that are often dif- 2003)that animals will retain the amino acids ficult for large Daphnia to ingest. Although these that are deficient in their food and metabolise may not present such a problem to diaptomids, those that are in excess. Thus, Daphnia that meet their relatively weak growth potential may delay their carbon intake requirements from planktic any substantial control on the dynamics of the foods that are (say) P but not N deficient, will larger algae. Under these conditions, there may retain relatively more of the P content than of the be limited scope for microbial pathways to re- N content, so that the N : P ratio of their excretory establish and for them to be exploited by abun- products is likely to be yet higher than that of the dant microzooplankton (including rotifers, such food intake. Thus, the nutrients that are recycled as Keratella and Polyarthra)orbysmall cladocer- do not necessarily assist in the correction of defi- ans, either feeding selectively (Bosmina, Chydorus ciencies in the growth environment of the food spp.). or by filtration in the nanoplanktic size organisms but rather accentuate them (see also range (perhaps involving small daphniids, such Sterner, 1993) (see also Section 5.4.5). as D. cucullata or Ceriodaphnia spp.). These organisms are frequently prominent in the plankton of Bottom--up and top--down processes in small eutrophic lakes (Gliwicz, 2003a) where they oligotrophic systems represent a third kind of interactive structure in During the late 1980s, there developed vehement the plankton. debate about whether phytoplankton biomass was controlled mainly by nutrients or by its graz- Feedbacks ing consumers. Both sides recognised that algal The nature of phytoplankton--zooplankton rela- biomass was not some continuous function of tionships is not without benefits passing in the thenutrients available and that herbivory was reverse direction. Perhaps the most important of capable of reducing phytoplankton biomass to these isthereturnoflimiting nutrients to the very low levels. The contentious issues were the medium as a consequence of the elimination of twin possibilities that consumers might contin- digestive wastes. This is not always a close loop, uously regulate producer biomass at artificially in so far as copepod faecal pellets presumably low levels or that low producer biomass is always fall some way before critical nutrients are cycled attributable to grazing. Most now seem to accept 288 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

that steady-state relationships are rare and that, sive consumers are accommodated, the potential within the bounds of normal variability, many oscillations become more complex but, at each outcomes are possible, under the influence of sev- step, the same supportive capacity is just shared eral factors that are not confined to resource sup- among more species representing more trophic ply and consumption. Although the debate has levels. The assembled linkages making up this receded, the vocabulary is permanently enriched food chain might well process and transport large (or, possibly, just stuck with) the adjectives masses of carbon (in the example, as much as 4- ‘bottom--up’ and ‘top--down’. Now these refer less -5 mg C L−1 a−1)but without ever raising the to ongoing controls and much more to the pro- aggregate biomass of the participating compo- cesses themselves -- the extent to which the bio- nents of the microbial food web above the sup- logical structure and function are shaped by the portive capacity. As it cannot be accumulated in resources or by the impact of consumers. More- the standingcrop, the carbon thus processed is over, the termsarenolonger applied only to phy- returned directly to the pool of dissolved carbon toplankton but are now used freely in the context dioxide pool and/or exported in the sedimentary of an implicit hierarchy of trophic levels. flux of faecal pellets and cadavers, to be returned So far as the original debate about controls less directly through local or global circulations is concerned, it is helpful to regard the issue in (Legendre and Rivkin, 2002a). terms ofsupportivecapacity. A low resource base These continuous severe constraints demand (whether determined by low phosphorus concen- that the trophic components, from the produc- trations in a lake, or very low iron concentrations ers and heterotrophic consumers right through in the sea, or low concentrations of combined to juvenile fish, are powerfully selected by their inorganic nitrogen in either, providing the addi- functional strengths and adaptations to deal tional resources needed to fix atmospheric nitro- with the rarefied resources (Weisse and MacIsaac, genare also rare) is absolutely inescapable. Thus, 2000). The overall control is within anyone’s on the basis of stoichiometry, a low concentra- understanding of ‘bottom--up’ regulation. Yet lit- tion of biologically available phosphorus (BAP) of tle other than trophic interaction controls the (say) 0.3 µgL−1 (10−8 M) cannot reasonably be relative masses of the components at any given expected to support more than a relatively small moment: small oscillations in the effectiveness biomass (in this case, perhaps 12--15 µgbiomass of calanoid feeding cascade through heavier pre- CL−1). Invested exclusively in phytoplankton, an dation on ciliates, better survivorship among the equivalent maximum concentration of chloro- nanoflagellates and harder cropping of the bacte- phyll a can be predicted (in this example, 0.2-- rial mass. Just as easily, fish feeding on calanoids 0.3 µgchla L−1), as can the adequacy to meet might trigger an effect upon ciliate numbers, theminimum requirements of fresh-water filter- depress the numbers of nanoflagellates, with feeders (here, it fails). Photosynthetically fixed cascading top--down effects on the balance of carbon that cannot be turned into biomass may algal and bacterial masses (e.g. Riemann and be wholly or part respired, with the balance Christoffersen, 1993). being excreted as DOC. This is, of course, useable substrate to bacteria, which, given their higher Bottom--up and top--down processes in affinity for the phosphorus, are sufficiently com- enriched systems petitive to be able to coexist with phytoplankton, Much the same model applies in oligotrophic yet withinthesamecapacity limitation on their lakes and seas, where top--down mechanisms reg- aggregate biomass. Both bacteria and small algae ulate the interspecific and interfunctional com- are liable to become the food of nanoplanktic position of the food web, even when the resource- phagotrophs and, thus, to be cropped down, but limited carrying capacity sets a powerful bottom- the same constraint on the total biomass per- -up constraint on behaviour. Where the bottom-- sists. In the three-component system, consumer up resource constraint is less severe, rather more abundance might alternate with food abundance latitude is available to fluctuations among the but only within the biomass capacity. As succes- components, with more opportunities to alter- CONSUMPTION BY HERBIVORES 289 native species and a greater variety of possible algae are more susceptible than large ones to responses. Raising the supportive capacity to (say) grazer control. Seasonal changes in the domi- 150 µgbiomass C L−1 (against 3 µgBAPL−1 nance of the phytoplankton, in the direction of or 10−7 M) opens the field to a greater aver- small to large algae, may be partly attributed to age biomass of more algal species, to alternative this mechanism (Sommer et al., 1986). means of harvesting and consuming them and, It is not always easy to separate the impact so, to a wider variety of consumers. Now the cas- of bottom--up resource control from top--down cading effects influence not just how much car- predator control on the abundance of Daphnia. bon is resident in which functional level but may We can point to the impact of low or zero fish play a strong part in selecting the survivors. populations, not just in limnetic enclosures, but Increasing the carrying capacity by another in natural lakes following some mass mortality order of magnitude (say, to 1.5 mg biomass of fish. Following the mortality of a major plank- CL−1,against∼30 µgBAPL−1)would take the tivore in Lake Mendota (cisco, Coregonus artedii), supportable system to well within the bounds Vanni et al. (1990) observed a big increase in of direct herbivory by filter-feeders and to the the Daphnia pulicaria over the previously more range ofthebest-known incidences of top--down abundant D. galeata,enhancing grazing pressure control of phytoplankton. The point is now well on the phytoplankton and bringing an extended made about the efficiency of direct consumption phase of clear water. and assimilation of a sufficient number of Daph- In this context, events in the mesotrophic nia feeding onphytoplanktersupto30--50µm North Basin of Windermere illustrate inter- is capable of grazing down the food resource annual fluctuations in the predominance of (including most of the heterotrophic bacteria, predation- and resource-driven forcing. George flagellates and ciliates too) to extremely low lev- and Harris (1985)noted that striking inter- els indeed, leaving the water very clear (Hrba´ˇcek annual differences in the numbers of Daphnia in et al., 1961; Lampert et al., 1986; Sommer et al., theplankton during June and July were inversely 1986)(seealso Fig. 6.8). Reynolds et al. (1982a) correlated with the temperature of the water in claimed this situation is unsustainable, at least June. The correlation with the biomass increase in the pelagic, unless alternative sources of food in the young-of-the-year (YOY) recruits of perch can be exploited, (say) in the littoral or sub- (Percafluviatilis)isweak, even though the latter littoral benthos. In the Blelham enclosures, no is broadly correlated with summer water temper- such alternative was available; the consequence atutes (Le Cren, 1987). The later analyses of Mills was the massive mortality of Daphnia,especially and Hurley (1990) confirmed only a small depen- among the most juvenile cohort (Ferguson et al., dence on annual perch recruitment. The stronger 1982)andacollapse in top--down pressures. Algae influence of the physical conditions on both the were able to increase again, at the expense of zooplankter and planktivore prompted deeper nutrient resources, before supporting the resur- studies that related the biological fluctuations gence of the next Daphnia episode. to subtle year-to-year variations in the annual What happens in many small, enriched lakes weather patterns. These are themselves driven by is that the tendency to stage these wide fluctu- significant year-to-year fluctuations in the posi- ations in the biomass of grazed and grazer is tion of the northern edge of the North Atlantic damped by planktivory. With many species of Drift Current (the ‘Gulf Stream’) (George and juvenile fish and the adults of some feeding obli- Taylor, 1995) and, especially, to interannual oscil- gately or opportunistically on zooplankton, the lations in the average atmospheric pressure dif- intensity of planktivory may fluctuate seasonally, ference between southern Iceland and the Azores in response to temperature, to the recruitment of (the now well-known North Atlantic Oscillation young fish and to continued food availability (e.g. or NAO) (Hurrell, 1995). Throughout Europe, lim- Mills and Forney, 1987). There are, nevertheless, nological behaviours are now being shown to be some top--down effects evident as the larger zoo- correlatives of the NAO (Straile, 2000; George, plankters are selectively removed and the smaller 2002). 290 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

So far as the linking mechanism in the variable magnitude and duration. However, if dynamics of Daphnia in Windermere are con- the duration of the opportunity is sufficiently cerned, Reynolds (1991)showedthat the years of extended, the control switches to the consumer, good recruitment coincided with the persistence becoming strongly ‘top--down’. of Asterionella in the plankton, as a direct consequence of the cool, windy weather associated in this region with the dominance of Atlantic Intervention in food-web interactions airstream. In warmer years, the earlier onset of As a footnote to this section, the nature of the thermal stratification robs the putative Daphnia existing or recent interreactivity of the food-web population of the one food source that is capa- components may be exposed not just by catas- ble of sustaining its growth and recruitment in trophic interventions (fish kills, spills of toxic this lake. Indeed, it was shown that the size substances, etc.) but also through the impacts of the Asterionella crop was less important than of successful invaders. The historic overexploita- was the last date in the year that its numbers tion of native piscivorous lake trout (Salvelinus in the surface water exceeded the threshold of namaycush)inLake Michigan and its susceptibil- adequacy to sustain the requirements of Daphnia ity to attack by the invasive sea lamprey (Petromy- (some 1300 cells mL−1,orclose to 0.1 µgCmL−1) zon marinus)ledtoacatastrophic decline in the (cf Table 6.3). Thereafter, other filterable algae top carnivore niche during the 1950s and to an were generally too few innumbertomakeupthe unopposed niche for the invasive planktivore the shortfall. alewife (Alosa pseudoharengus) during the 1960s Clearly, peak Daphnia numbers in any indi- (Christie, 1974). A rigorous programme of lam- vidual year will have been influenced by size of prey eradication and salmonid restocking, helped the overwintering stock, its early rate of recruit- by several severe winters, brought a substantial ment and to the feeding choices of the stand- reduction in the alewife populations (Scavia and ing fish stock. The point is that the years of suc- Fahnenstiel, 1988). There were significant reper- cessful recruitment of the Daphnia are strongly cussions in the lower trophic levels, notably an influenced by the coincidence of bottom--up and increase in large-bodied Daphnia pulicaria,abso- top--down forces blending in a fortuitous manner. lutely and relative to small-bodied zooplankton The food resource and the exploitative potential (Evans and Jude, 1986). Water clarity improved as of the Daphnia are the most reliable of the many phytoplankton was cropped more heavily, aggre- stochastic variables that bear upon the quanti- gate abundances actually paralleling the changes tative strength of either their precise timing or in the alewife numbers (Brooks et al., 1984). whether these coincide significantly or at all. Growing strength in the recruitment and Thus, great interannual variations in the net pro- near-shore activity of yellow perch (Perca duction and recruitment to pelagic communities flavescens) has since obscured one set of cascad- of particular locations in seas and lakes come to ing effects and superimposed another. There depend upon the interaction of small and more have been other spontaneous changes among subtle interannual variations. This is, in essence, the lower trophic levels triggered by other the ‘match--mismatch hypothesis’ advanced by alien introductions, notably the mesoplank- Cushing (1982)toexplain interannual fluctua- tic carnivorous cladoceran Bythotrephes, which tions in the breeding success of fish of com- has established itself through much of the mercial importance. It is an extremely important Laurentian Great Lakes (Lehman and Caceres,´ principle of population and community ecology. 1993)and by the zebra mussel, Dreissenia poly- Its workings can be explained retrospectively and morpha. Though essentially benthic, the huge its outcomes can be anticipated on a probabilistic aggregate filtration capacities represented by basis but precise outturns cannot be predicted. well-established populations of the bivalve have The sketches in Fig. 6.10 summarise a series of measurable effects on the planktic food web of possibilities of bottom--up tracking responses to lakes as large as Lake Erie (Beeton and Hageman, aroutinely pulsed resource opportunity but of 1992;Holland, 1993). CONSUMPTION BY HERBIVORES 291

Figure 6.10 (a) The (bottom–up) responses of a consumer to a regularly pulsed supply of resource but of varying magnitude relative to its requirement and, thus, of exploitative opportunity. In (b), the resource availability is absolutely greater and of longer duration; the opportunity is such to allow the consumer to control resource availability (from the top–down). Redrawn with permission from Reynolds (1991).

Food-chain length consumers were to achieve a transfer efficiency of The examples given attest to the importance of even 20%, the rate of dissipation of the potential the web of interacting consumers in affecting the energy (mainly as heat) through a producer → biomass and species composition of the producer herbivore → carnivore sequence means that the base. In later sections, the role of the food web in investment in carnivores is probably already less regulating of ecosystem functions, resource stor- than 30 g C m−2 a−1.Extension of this argument age and recycling, and the yield to commercial suggests that the available food base becomes so fisheries will be evaluated. The growth in appre- diluted that it is impossible to support more than ciation of the complex mechanisms has neces- four or five links. Energy-based food webs are sup- sitated a substantial rethink on the number of posed to be constrained by the number of times viable linkages in the web and the flows of mate- is moved up to the next trophic level (Cohen et al., rials and energy across them. Conventional eco- 1990). logical energetics developed and perpetuated the Recent studies (Spencer and Warren, 1996; case that food-chain length is determined by the Vander Zanden et al., 1999;Postet al., 2000a;Post, stability of the key components and by the avail- 2002a) using experimental enclosures and stable- able resource base and the usable energy influx. isotope analyses, have shown the need to adopt From a given solar area-specific energy input, an alternative metric for describing food-web investment in carbon bonds and the high cost structure. This is based on the strength of compo- of its transfer upthefood chain, there is plainly nent interaction (which reflects the food choices little ‘left’ after just a few links. In Section 3.5.2, that are actually made) and the measurement of it was argued that the net photosynthetic pro- dominant food-chain linkages. Neither resource duction of 50--800 g C m−2 a−1 represented an availability nor dynamical constraints play a con- energy investment of 2--32 MJ m−2 a−1,orless trolling role in these functional measures. On the than 2% of the PAR flux available. If successive other hand, it is the size of the ecosystem and the 292 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.11 Comparison of the changes in the standing crops of vernal Asterionella populations ( t)in Crose Mere, UK, during consecutive years, in relation to the absolute concentrations of infecting spores and sporangia of the chytrid parasite Zygorhizidium afﬂuens ( d). The percentages of host cells infected and the water temperatures are also plotted. Redrawn from Reynolds (1984a).

totality of its resources that have emerged as the poorly known, although the work of few spe- crucial determinant of chain length in aquatic cialist investigators shows that it should not be food webs (Post et al., 2000b). Whereas just two or underestimated, for the effects of fungal attack three trophic levels can be accommodated in very and bacterial lysis that have been reported are small aquatic systems, from the phytotelmata of indeed impressive. plant foliage to small pothole lakes (10−3 to 102 m3), the linkages increase and become succes- 6.5.1 Fungal parasites sively more varied and adaptable in small lakes Most fungal parasites of phytoplankton belong to (105 to 108 m3), large lakes (1012 to 1014 m3)and theorder Chytridiales or are biﬂagellate mem- oceans (1016 to 1017 m3)(Post,2002b). bers of the Phycomycetes (see the review of Canter, 1979). Moreover, infections can ascend to epidemic proportions, becoming the proximal 6.5 Susceptibility to pathogens and cause of death of large proportion of the extant hosts (Canter-Lund and Lund, 1995). However, it parasites is often the case that separate instances of infection but ones that involve the same species of The existence of pathogenic organisms and para- hosts and parasites nevertheless result in quite sitic fungi and protists capable of infesting plank- different mortality outcomes (see Fig. 6.11). Some tic algae and causing their death has been known of the most exhaustive investigations of the foralong time. The range of the relationships epidemiology and ecology of fungal infections that they strike with their planktic ‘hosts’ is of phytoplankton have been carried out in the wide. On the one side, it may beaformofher- English Lakes, where chytrid infections of domi- bivory, where the animal lives within the body nant diatoms had been observed from the outset of the plant, like the rhizopods which inhabit of the research on phytoplankton dynamics. This fresh-water Microcystis colonies (Reynolds et al., early work established the identities of some of 1981)ortherotifers such as Cephalodella and Hert- theparasites and the general correlation of the wigia, which (respectively) eat Uroglena and Volvox dynamics of their infectiveness with the environ- from the inside out (Canter-Lund and Lund, 1995; mental conditions governing other aspects of the van Donk and Voogd, 1996). At the other, there dynamics of their hosts. They also showed that, in are obligately parasitic fungi (Sparrow, 1960; the case of Asterionella in Windermere, parasitism Canter, 1979;Canter-Lund and Lund, 1995)and was not merelyaconstraint on the dynamics of pathogenic bacteria and viruses (Bratbak and Hel- thespring bloom but a signiﬁcant control on size dal, 1995;Weisse, 2003). The role played by these and species composition of the smaller autumn agents in reducing host biomass is, in general, bloom (Canter and Lund, 1948, 1951, 1953). SUSCEPTIBILITY TO PATHOGENS AND PARASITES 293

The most conspicuous fungal parasites on particular, hosts need to be numerous and spores Asterionella belong to the genera Rhizophydium have to be infective for the parasite to take hold. and Zygorhizidium, which also infect many other Of special interest is the fact that, under condi- groups of fresh-water phytoplankters. It is gen- tions of low light or darkness, infective zoospores erally difficult to distinguish among individ- are not attracted to potential host cells of Asteri- ual species except as a consequence of their onella as they are in good light. They rarely attach host specificity. In the presence of multi-species to the host cells and are quite ineffective in the planktic assemblages, the incidence of infec- dark. tive chytrids will usually be confined to just The effects of light on the infectivity and one of them: ‘fungal parasites are excellent tax- development of the parasite contribute to the onomists’ (J. W. G. Lund, personal communica- complexity of the circumstances of epidemic ini- tion). Individual genera are separated on the basis tiation. The condition of both hosts and parasites of sporangial structure, dehiscence, spore char- formed a key part of Bruning’s (1991a, b, c)sys- acters and mycelial development. Zygorhizidium tematic investigation of the response of infectiv- species constitute epidemics on mucilage-bound ity to light and temperature. Under low levels chlorophytes such as Coenochloris, Chlamydocapsa of light, with algal growth constrained, fungal and Pseudosphaerocystis. Rhizophydium species also zoospores of Rhizophydium are only weakly infec- occur on Eudorina,ondesmids and on the cysts of tive. On the other hand, the greatest production Ceratium.Cyanobacteria such as Anabaena are var- of zoospores (as spores per sporangium) occurs at iously attacked by chytrids of the genera Blasto- ∼2 ◦C. Production is light saturated at ∼100 µmol cladiella, Chytridium and Rhizosiphon.Otherspecies photons m−2 s−1 over a wide range of tempera- of Chytridium are found on Microcystis,oncertain tures. Regression equations were devised to deter- desmids (including Staurodesmus)anddiatoms mine the development times of sporangia and (including Tabellaria). Pseudopileum infects chrys- thesurvival time of infective spores. Thence, the ophytes such as Mallomonas. Podochytrium is rep- limiting frequency of hosts (Asterionella) could be resented by species that parasitise diatoms. In calculated. By plotting the (‘threshold’) concen- all these instances, infective spores are dispersed trations required to facilitate (a) a positive infec- in the medium, are attracted to and attach tion development rate of growing hosts and (b) themselves the cells of host organisms, where spore suvival, Bruning (1991c)discerned the envi- they establish absorptive hyphae into the host ronmental conditions most likely to lead to epi- cells, enlarge and develop new sporangia. The demic infections. The plot of epidemic thresholds host cells are almost always killed. Epidemics of host densities of <200 cells mL−1 (Fig. 6.12a) will destroy a large number of host cells and shows a plateau at temperatures above 7 ◦Cand impinge on the dynamics and perennation of the at light intensities down to ∼15 µmol photons hosts. m−2 s−1, which values are mildly limiting to host Elucidation of the host--parasite relationships growth. This area extends into the lower left cor- that impinge upon the ecology of phytoplankton ner of low light and temperature but it is oth- could progress only so far on the basis of observa- erwise bounded by steep gradients of increas- tion. Real advances came once it had become posing thresholds, where low light or low tem- sible to isolate the fungi and to maintain them in perature preclude epidemic development (areas dual-clonal cultures (Canter and Jaworski, 1978). shown in black). The minimum threshold, i.e the In a series of remarkable experiments and obser- conditions most amenable to epidemic, occurs at vations, Canter and Jaworski (1979, 1980, 1981, ∼11.0 ◦Cand∼19 µmol photons m−2 s−1 (which 1982, 1986)didmuch to explain the life cycles conditions might support a host growth rate of of Rhizophydium planktonicum emend., Zygorhizid- ∼0.66 d−1). The contours in Fig. 6.12b show the ium affluens and Z. planktonicum, host range, host- host density necessary to parasite survival. The -parasite compatibility, zoospore behaviour in lowest threshold values, indicating optimum con- relation to light and darkness and the variabil- ditions for the persistence of the parasite within ity governing the onset of fungal epidemics. In the host population, are encountered under 294 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.12 Effects of light and temperature on the occurrence of Rhizophydium on Asterionella. Contour lines represent the thresholds of host concentration in cells mL−1 for (a) the development of epidemics and (b) for the survival of parasites. Redrawn with permission from Bruning (1991c).

conditions of saturating light and low temper- around the prey organism (often a centric atures. Respite from parasites under low light or diatom). They fall empty and transparent and in darkness may assist host survival. the whole becomes surrounded by mucilage, Other parasites and hosts possibly strike anal- as the animal contracts to an ornately spined ogous relationships but the details must be cyst. Digestion of the food proceeds until one or expected to differ. Looking again at the plots in more small amoebae emerge from the cyst, to Fig. 6.11,the observations on Zygorhizidium are recommence the life cycle. Towards the end of a compatible with the Bruning model for Rhizo- period of abundant hosts, the contents of some phydium infectivity but the better Asterionella sur- maturing digestion cysts, instead of releasing vivorship in 1967 as compared to 1968 clearly amoebae, are transformed into a rounded resting benefitted from the later intervention of the par- spore. The animal can survive in this condition asite into the host growth cycle. for many months until hosts once again become It is also appropriate to recall that host-- abundant. parasite relationships may be confounded by fac- Vampyrella is another interesting amoeboid tors other than the ‘normal’ behaviours of the rhizipod that uses its slender pseudpodia to proximal players. One of these is host hypersen- attach to the cells of algae (usually filamentous sitivity (cf. Canter and Jaworski, 1979)toinfec- chlorophytes such as Geminella)butnottowrap tive spores, where algal cells die so soon after around its prey. Instead, Vampyrella dissolves a lit- infection that sporangia fail to develop and tle area of host cell wall and extracts (‘sucks out’) the progressoftheepidemic becomes stalled. the contents of the host cell into its own body. It Another is the remarkable phenomenon of may suck out another host, perhaps simultane- hyperparasitism: Zygorhizidium affluens,forexam- ously, before turning itself into a digestion cyst ple is itself frequently parasitised by another (though, in this genus, it is not spined). The cysts chytrid, Rozella sp. (Canter-Lund and Lund, 1995). eventually break to release new infective amoebae or a resting spore. Species that attack other 6.5.2 Protozoan and other parasites algae also seem to excise similar holes in the host The dividing line between a consuming cell wall. It also appears that individual vampyrel- phagotroph and true parasite is a fine one. lid species are usually consistent in their choice Whereas the typical feeding mode in amoebae of hosts (Canter-Lund and Lund, 1995). involves the pseudopodial engulfing of food Canter-Lund and Lund (1995)alsogave organisms and intracellular digestion from details of an aberrant, plasmodial organism afood vacuole, the amoeboid Asterocaelum that attaches to Volvox colonies and sets up a comprises of little more than a few long, fine mycelial-like network, consuming individual host pseudopodia. According to the description of cells as it grows inexorably through the colony. Canter-Lund and Lund (1995), these are wrapped These will extend beyond the host confines, SUSCEPTIBILITY TO PATHOGENS AND PARASITES 295 presumably, to facilitate transfer to another. Then, as reports of minimal abundances of Canter-Lund and Lund (1995)believe the alga to virus particles in various aquatic environments, be one of the slime moulds, or Myxomycetes. ranging between 104 and 108 mL−1 (Torella and Most of the non-fungal parasites (and many Morita, 1979;Berghet al., 1989;Bratbak and of the fungi too) escape without mention in Heldal, 1995)began to accumulate, more interest many ecological studies of phytoplankton. This in the ecological importance of viruses has been may reflect a true rarity but it seems unlikely registered. that the profusion of parasites is confined to the Modern methods of ennumeration invoke sites where their presence has been diligently plaque assays, epifluorescence microscopy and sought. Thus, it is difficult to form an objective flow cytometry, using DNA-specific stains. Viruses view of the role of losses to parasitic attack in are more numerous in lakes than in the sea and the population dynamics of phytoplankton gen- their abundance in lakes is said to broadly corre- erally. In terms of carbon pathways and sinks at lated with chlorophyll content and the numbers the ecosystem scale, the probability is that para- of free-living bacteria; the likely causal connec- sites interfere little, as infected hosts are con- tion is trophic state. According to Maranger and sumed as are the uninfected algae, while the Bird (1995), viral abundance among the Québec survivorship of host propagules may be such to lakes they studied was most closely correlated prevent local elimination from participation in to bacterial production. This they considered subsequent bursts of growth and recruitment. to be indicative of the greater dependence of At thelevel of individual species, however, par- fresh-water microbiota on allochthonous organic asites can exact a high cost in terms of domi- materials. nance. From being the regular summer dominant Viruses are responsible for phage-induced of the phytoplankton in Esthwaite Water from mortality of bacterial and cyanobacterial hosts the1950s to the early 1980s (Harris et al., 1979; but the literature considered by Weisse (2003) Heaney and Talling, 1980b), Ceratium was all but shows enormous variability (from 0.1% to 100%). eliminated by a sequence of parasitic epidemics He points out that differing assumptions and (Heaney et al., 1988). An infection of the overwin- conversions distort a clear picture. Regulation of tering cystsbyaRhizophydium species, may have themicrobial community is yet harder to demon- been the ‘last straw’ as it reduced the algal inocu- strate.Virus--host interactions are host-specific lum to extremely low numbers. It was not until and dynamic. Hosts may be virus-resistant; themid-1990s that Ceratium began tobecome viruses may be dormant for long periods between once again abundant in the lake (although, as infective opportunities. Viruses may even ful- at 2003, still in subdominant numbers). fil a positive role in microbial food webs by releasing and recycling nutrients and dissolved organic matter from lysed cells, so stimulating 6.5.3 Pathogenic bacteria and viruses new bacterial production (Thingstad et al., 1993) The existence of viral pathogens (see also Fig. 6.13). Much remains to be elucidated (‘bacteriophages’: Spencer, 1955;Adams, 1966; about the net role of viruses in the dynamics of ‘phycoviruses’: Safferman and Morris, 1963; phytoplankton. ‘cyanophages’: Luftig and Haselkorn, 1967; Algal-lysing bacteria have also been isolated Padan and Shilo, 1973) infecting bacteria (includ- from a variety of fresh-water habitats -- including ing Cyanobacteria) and eukarytoic algae has sewage tanks -- where they attack a wide range long been recognised. In some cases, they had of algae. A few affect planktic genera but there is been isolated from field material and have been no known host specificity. Most of the identified found to be capable of lysing laboratory strains species are gram-negative myxobacteria that pro- of host organisms. Until recently, however, the duce a variety of hydrolytic enzymes, such as cel- occurrence of the organisms had been regarded lulases, capable of lysing other microorganisms as rare and their isolation in the laboratory (Shilo, 1970; Daft et al., 1975;Atlas and Bartha, had scarcely been attempted (Weisse, 2003). 1993). 296 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Aqualification to this statement is necessary in the context of cells sinking ‘irretrievably’ into deep water. Treated as ‘losses to sinking’, settling cells surely constitute a dynamic sink but it is not settlement that is lethal. Unless the settling cells are able to enter a physiological resting state (as do the vegetative cells of several species of centric diatom and the many types of dormant propagules, considered in Section 5.4.6), cells leaving thephotic layers are likely just to respire themselves away. In deep water columns, especially during late autumnal mixing at high latitudes, much of the residual phytoplankton biomass in suspension becomes similarly unsustainable on thelight energy available. Cells die and become Figure 6.13 Diagram of the relationships among microbial liable to decomposition. This may be adjudged to components of the plankton (including viruses) and the pool be non-beneficial to the survival of given species of dissolved organic matter (DOM). HNF, heterotrophic but the saprophytic oxidation of cell material nanoflagellates. Redrawn with permission from Weisse and the re-solution of its mineralised compon- (2003). ents are key aspects of pelagic resource recycling. Whether material recycling occurs substantially in the water column or mainly after the bulk of the algal biomass has once settled to the 6.6 Death and decomposition bottom is critical to the rate of resource renewal. Settled material may resuspended before it is It has been implicit throughout the present chap- finally decomposed and thus play some part in terthat the mortality of primary producers is therestoration of reusable resources to organ- explained principally in terms of biomass losses isms still in the trophogenic water layers. If not, to other agents or to other compartments of the carbon and nutrient cycling may be governed by ecosystem. Spontaneous death -- the failure of the redox transformation and solute diffusion. organism to maintain its basic metabolic func- It is relevant to refer here to the rates tions -- as a consquence, for instance, of resource of phytoplankton disintegration and decompo- exhaustion or light deprivation, is rarely consid- sition. There are reasonably attested allometric ered as an issue. It has to be admitted that there exponents of basal metabolism (Section 5.4.1) is some difficulty in discerning satisfactorily the to describe the cell-specific consumption of cell boundaries between loss of vigour and physiolog- carbon in self-maintenance through dark peri- ical close-down, or between dormancy and struc- ods, generally falling within the order of magni- tural breakdown. From my own experiences of tude 0.01 to 0.1 d−1. The stoichiometric demand tracking the dynamics of populations through of oxidising 1--10% of the cell carbon each day temporally sequential cycles, I am bound to a approximates to 0.03--0.3 mg oxygen (mg cell C)−1 view that unless an algal cell wall is entirely d−1.For night-time algal respiration to consume devoid of contents, which are not manifestly the air-equilibrated oxygen content of a water −1 those of some invasive parasite or saprophyte, column (say 8--9 mg O2 L )requires the pres- then it is not safe to assume that it is dead and ence of algae at a density equivalent to ∼30 incapable of physiological revival. Equally, when mg cell C L−1,orroughly 600 µgchlorophyll theother ‘traditional’ causes of mortality are L−1. This may give some comfort to the many fully quantified and attributed, the proportion managers of lakes, reservoirs and fishponds who that is otherwise unaccounted and, so, ascribed become perplexed about the consequences of oxy- to cell death, is usually small. gen depletion by phytoplankton crops: their fears AGGREGATED IMPACTS OF LOSS PROCESSES 297 are probably exaggerated. However, in water bod- sure of homeostatic function in the face of ies already experiencing a significant biochemi- chaotic enviromental variability. cal oxygen demand (BOD), the additional burden of a sudden physiological collapse and decomposition of phytoplankton might, indeed, push the 6.7 Aggregated impacts of loss oxygen dynamics to levels beyond the survival of processes on phytoplankton fish and other animals. The principal agents of decomposition are composition saprophytic bacteria and other microbial heterotrophs. The main groups of decomposer organ- The foregoing sections demonstrate that the rates isms, the organic carbon compounds that they of biomass loss sustained by natural populations oxidise (various carbohydrate polymers, proteins, of phytoplankton are comparable with and, at fatty acids and lipids) and the relevant enzymes times, exceed the scale of the anabolic processes that are produced are the subject of a useful that lead to the increase in biomass. Loss pro- review by Perry (2002). The rates of algal decom- cesses are important in determining whether and position have been reported in at least two dozen when given species will increase or not. Moreover, studies that have been published since the care- different species-specific partitioning of losses ful experiments of Jewell and McCarty (1971). must play a major selective role in influencing Mostly these conform closely to the original day-to-day variations in the assembly and species deductions and statements. The labile materials dominance of the whole community. To be clear, that are readily respired and which account for loss processes affect only extant populations, the about one-third of the carbon content of the presence of which is subject to the two over- healthy cell will probably havebeenoxidised riding conditions that no alga will be conspic- prior to death. Much of the carbon remaining in uous in the phytoplankton unless (i) it has had the cadavers takes up to a year to oxidise but a both the opportunity and the capacity to exploit fraction, comprising mostly structural polymers, the resources available and (ii) that the extent to including cellulose-like compounds, decomposes which its specific light, temperature and resource at only a few percent per year. First-order kinet- requirements for recruitment by growth are met ics describe these processes quite comfortably: is at least as favourable as, if not better than, that depending upon temperature, the exponents for of any of its rivals. Within these twin constraints, oxidative carbon decay generally vary between seasonal variations in the magnitude and parti- 0.01 and 0.06 d−1. tioning of species-specific losses contribute to the As a footnote to this section, it is proper to net dynamics of waxing and waning populations, point to some recent findings concerning pro- which are the driving mechanisms of phytoplank- grammed cell death. Among microorganisms, ton periodicity. perpetuation of the genomic line may be assisted Put in its most basic qualitative terms, inten- by the sacrifice of quantities of vegetative cells. sive direct filter-feeding may well suppress the Examples include the differential material invest- net increase rates of nanoplankters and of small ment in the survivorship of overwintering cells microplankters and favour the recruitment of of Microcystis at the expense of many that die larger algae instead. Similarly, contraction in the during the benthic life-history stage (Sirenko, depth of the entrainment by fully developed tur- quoted by Reynolds et al., 1981)andthereported bulence immediately selects in favour of small or unequal allocation of biomass between daugh- motile species at the expense of larger non-motile ter cells of dividing Anabaena,toimposeaself- species, settling downwards following the loss of control on population growth rate (Mitchison suspension. In many instances, the differential and Wilcox, 1972). Carr (1995)believed that the sensitivity to losses has an intrinsic seasonality genetically programmed process of cell destruc- of its own. In one of the earliest attempts to bud- tion, or apoptosis,isprobablyemployedwidely getthe fate of primary products in a lake, Gliwicz among microbes in order to achieve some mea- and Hillbricht-Ilkowska (1975)deduced that most 298 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

Figure 6.14 Comparative sensitivities of net increase rates of three phytoplankters (Ast, Asterionella; Chlo, Chlorella; Mic, Microcystis), each growing at their maximal rates under 12-h : 12-h light–dark alternation, to (a) dilution (q being the volume displaced each day from a water body of volume V), (b) sinking losses (hm being the thickness of the mixed layer) and (c) ﬁlter-feeding (F being aggregate volume ﬁltered each day). Redrawn from Reynolds (1997a).

of the spring production in small, eutrophic, tem- suggested in Section 6.1), the processes balance perate Jezioro Mikolajske was eliminated by sed- out, so that biomass carry-over and its mean imentation. The summer production largely sus- standing crop are estimable outcomes of the sys- tained the zooplankton while, in the autumn, temthat supports them. At the level of species most of the primary product was submitted to and species-specific dynamics, however, loss pro- decomposition. The observations dovetail with cesses discriminate among them and play a quan- the perspective of alternative survival strategies tifiable part in selecting among the species aspir- of phytoplankton (see p. 210 and Box 5.1). Thus, ing to increase their populations. The large inter- thevernal plankton is selected broadly by the (R-) specific differences in the sensitivity of phyto- trait of exploitation of turbulent mixing and its plankton to potential loss mechanisms are exem- tolerance oflowlight and is vulnerable to density plified in Fig. 6.14. This has been devised to illus- stratification. Early-summer (C-) plankton is effi- trate the discriminatory simultaneous effects of cient in quickly turning resources to biomass but separate alterations in flushing rate (qs/V), mixed- is usually vulnerable to herbivorous consumers. layer depth (hm)andtheaggregate filtration Late-summer plankton has more of the conser- rate (Fi)ofthe zooplankton community upon vative (S-) characteristics of resisting sinking and three contrasted quite different phytoplankton grazing to the limits of its (albeit diminishing) species: Chlorella (representative of C strategists), sustainability. Asterionella (R)andMicrocystis (S). Each has been Self-evidently, populations increase, stagnate accorded a positive rate of replication, being that or decrease in consequence of the relative quan- generated for a 12-h day of saturating light inten- tities of the positive and the negative exponents sities and nutrient supplies at 20 ◦C. Despite hav- applied. Over substantial periods (≥1yearwas ing the slowest potential rate of growth, which AGGREGATED IMPACTS OF LOSS PROCESSES 299

prevents it from increasing at all in the face of Asterionella A moderate flushing, Microcystis nevertheless out- Asterionella B (Apr) performs Asterionella,underconditions of near- surface stratification, and Chlorella when subject Asterionella B (Jul) to intense grazing pressure. Asterionella B (Sep) Reference back to Eq. (5.1)reminds us that Fragilaria A (season) ratesapply to standing inocula of varying sizes Ankyra A (Jul) (N0)andaffect realised populations (Nt). A large, Ankyra A (Aug) dominant population of Asterionella can still be Chromulina B dominant the next day, even when it has been subject to greater net loss rates than all other Cryptomonas A (Aug) species present on the preceding day, simply by Eudorina A (May) virtue of the large ‘inoculum’ carried over. How- Eudorina B (May) ever, if uninterrupted, this process of attrition Microcystis A (season) in the face of net gain by another is certain to 0 50 100% lead, eventually, to its replacement. This principle is developed later (see Section 7.3.1). For KEY GSO the present, it is sufficient to distinguish the dynamic processes from their effects. Most plank- Figure 6.15 Graphical representation of the loss budgets. tonbiologists will accept the differences in the Each horizontal bar represents the gross cell production of vulnerabilities of different kinds of phytoplank- the named populations in the Blelham enclosures during ton to commonly imposed constraints. Some, 1978. Appropriate shading (as shown on key) represents the however, seem to have difficulties in accepting minimum proportions that were grazed (G), sedimented (S) that it is possible for small algae and grazers to or were otherwise lost from suspension (O); intermediate coexist, and for Daphnia still tostarvewhen fil- shading represents the mutual overlapping of confidence terable algae and bacteria are present in water intervals about the determinations. Modified and redrawn samples submitted to microscopy. with permission from Reynolds et al. (1982a). This may also be the right place to emphasise that it is the properties of the actual organ- of the surface mixed layer that is critical to sus- isms in relation to the contemporaneous environ- pension. mental conditions that are decisive. These may, The quantitative studies of phytoplankton at times, outweigh behavioural differentiations losses in the Blelham enclosures have been men- anticipated by taxonomic identity alone. Thus, tioned on several occasions in the development although it is perfectly justifiable to suggest of this chapter. Among the outcomes were the that mature Microcystis colonies are quite unman- interspecific comparisons of season-long loss par- ageable and reputedly unsuitable as food for titioning of phytoplankton losses. These are cited most crustacean zooplankters, a substantial pre- to provide an appropriate closing illustration of existing population of filter-feeders is quite able thedifferential sensitivities of phytoplankton to to suppress the onset of Microcystis dominance. thevarious processes. The horizontal bars in This is attributable to the successful removal Fig. 6.15 each represent the total production of by grazers of small colonies in their recruiting the species named (calculated as P, according to (infective) stages faster than they can grow (say, Eq. (6.20)) in the named location and during the −1 rG ≥ 0.3 d ). Neither is there any paradox that specified phase of growth or attrition. The min- diatoms should increase in number when a large, imum fractions of each product that were lost deep lake or the sea begins to stratify and inocula to grazing, settlement and ‘other’ sinks (lysis of are entrained over subcritical depths (Huisman Microcystis in Enclosure A, gametogenesis of Eudo- et al., 1999), yet populations decline abruptly when rina)areshown. Despite the width of the confi- asmallonestagnates (Reynolds, 1973a;Reynolds dence intervals, the contrasted fates of specific et al., 1984). In both cases, it is the absolute depth production are immediately apparent from the 300 MORTALITY AND LOSS PROCESSES IN PHYTOPLANKTON

representations. Not less than 80% of the ver- of whole cells). These processes are the subject nally produced Asterionella cells in Enclosure A of Chapter 6. and B were eliminated through sinking, with Wash-out, especially in continuously and any balance being lost to grazers. On the other intermittently flushed systems, sedimentation of hand, >87% of the cells of Ankyra produced in disentrained cells and grazing by filter-feeders Enclosure A, >95% of the Chromulina produced can each account for major losses of phytoplank- in Enclosure B and probably 100% of the Crypto- tonbiomass. The dynamic effects of each can monas produced in either were removed by her- be described by exponential-decay functions, bivorous zooplankters. Grazing also eliminated analogous to dilution, and be expressed in the between 71% and 98% of the Asterionella produced same, summable units as cell replication, which in Enclosure B during July but <78% of the Frag- is a boon to simulation models of phytoplankton ilaria that were produced in Enclosure A. Prior population dynamics. The processes discriminate to gametogenesis, Eudorina seemed to have been among species and, hence, contribute to the less susceptible to grazing (<5% and <9% of the selection of species in given environments. products of A and B respectively). Zygotic spores In theory, hydraulic flushing affects all and spent male colonies did settle out at the entrained species to the same absolute extent but end of the population though the latter were faster-growing species are better adapted to main- already in an advanced state of decomposition tain themselves against dilution. Slow-growing, and disintegration. The Microcystis produced in larger algae tend not to be represented in the Enclosure A remained loss-resistant until a signif- phytoplankton of rivers (potamoplankton) unless icant surface scum formed overnight (on 20/21 the rivers are long and have high retentivity. September) and many cells were destroyed by Species which, for reasons of size or den- lysis. Autumnal sedimentation as viable colonies sity difference, are most readily disentrained accounted for the fraction (∼44% of the total pro- from turbulent layers and are simultaneously duction) that survived bloom formation. Of the unable to swim or regulate their densities, are Microcystis produced in Enclosure B, a large pro- vulnerable to sinking losses in water columns portion left the enclosure following a mechanical experiencing weakened mixing and reduced collapse of the buoyancy collar holding up the mixing depth. Sinking losses of planktic diatoms enclosure wall (7 September 1978). The residue, may considerably exceed the rates of recruitment plus a modest recruitment through new growth, by replication. The losses are not necessarily wholly sedimented as viable colonies. For further permanent and it is suggested that, in certain cir- details of these populations, see Reynolds et al. cumstances (e.g. dielly stratifying systems at low (1982a). latitudes), rapid sinking can be positively beneficial if later mixing is sufficiently vigourous and regular to return diatoms to the water surface. 6.8 Summary Several modes of herbivory characterise the phagotrophic exploitation of the plankton. Bac- The fate of gross planktic primary production is teria and picophytoplankton normally occur in divided between consumption and excretion at concentrations that offer poor energetic return the level of physiological homeostasis (basal res- for foraging effort. They are, however, harvestable piration, maintenance, voiding of unassimilable by theprotists (nanoflagellates and microciliates) primary photosynthate, considered in Chapter that constitute a microplanktic--microbial food 3). The materials accumulated and invested in web, which is itself cropped by mesoplanktic thegrowth and replication of new cells experi- (typically calanoid) consumers that feed effi- ence further losses to mortality and removal of ciently on selected items of food. Nanoplanktic fully formed individuals (through the wash-out, and microalgae, if they can be sustained in sinking, consumption by animals, disruption by sufficient concentrations (above a threshold of parasites and pathogens and physiological death ∼0.1 mg C L−1), represent an alternative food SUMMARY 301 resource that is available to direct consumption generally favours the larger, more efficient by filter-feeders. herbivorous filter-feeders. Fish predation selects Filter-feeding is an efficient and effective against large, visible filter-feeders but, presum- wayofforaging, provided the foods are of fil- ably, only when the zooplankters also occur in terable size and sufficiently concentrated above sufficient numbers to attract consumer attention threshold levels. While these conditions are away from other, more rewarding food sources. satisfied, cladoceran filter-feeders can flourish, Phytoplankton--zooplankton relationships vary reproduce and recruit, potentially quite rapidly, with trophic state and with the presence and new consumers to the assemblage. Two or more predilections of fish. generations may be recruited over a period of a Algal populations are susceptible to epi- month or so, each time raising several-fold the demics of fungal parasites. Far from being rate of grazing loss experienced by ingestible stochastic events, the susceptibility of hosts to species of phytoplankton. However, the aggregate infection and the conditons favouring epidemics filtration results in increasingly unsustainable are now broadly predictable. loss rates to the recruiting algae and which, once Descriptions of the destructive impacts of surpassing the rate of cell replication, can thus virus attacks on algae, cyanobacteria and bac- bring about the collapse of the food source. All teria have been appearing in the literature for filterable particles, including the components of over 40 years but it is barely more than a decade the microbial loop, can be very quickly cleared since their general abundance in waters (104 and from the water, leading to its high clarity. Other 108 mL−1) has been appreciated. The ecological things being equal, starvation and mortality role played by so many potential pathogenic of the herbivores results in a respite for the organisms is still not wholly clear. producers, which may increase in mass before Quantifiable effects of loss processes are the nextcycleofconsumptive tracking. assembled and compared at the end of the The presence of facultatively or obligately chapter, showing how potential changes in algal planktivorous fish may damp down considerably dominance respond to seasonally varying rates thepotential fluctuations in feeding pressure of population depletion experienced by different on the phytoplankton. Resource competition species. Chapter 7

Community assembly in the plankton: pattern, process and dynamics

7.1 Introduction 7.2 Patterns of species composition and temporal In the pelagic, as in the great terrestrial ecosys- change in phytoplankton tems, space is occupied by numbers of organisms of various species forming distinct pop- assemblages ulations fulfilling differing roles. Of course, these assemblages of species reflect autecological 7.2.1 Species composition in the sea aspects of preference and tolerance but they also Despite the mutual contiguity of the marine show many synecological features of the mutual water masses on the planet, the composition specific interactions and interdependences that and abundance of the phytoplankton show broad characterise communities. The numbers of organ- and significant variations, both in space and isms, the relative abundances of the species, through time. To provide some sort of review their biological traits and the functional roles and then to offer a classification of the patterns that they fulfil all contribute to the observ- are formidable objectives. In setting out to ful- able community structure.Intheplankton and fil the present requirement, I am aware, on the in other biomes, the challenge to explain how one hand, of the large body of mainly miscel- these structures are put together, how they are laneous information culled from the detailed then regulated and how they alter through time, records of particular sea cruises and, on the falls withintheunderstanding of community other, of the several monumental syntheses that ecology. have heroically attempted to sort, to classify This chapter considers the structure of phyto- and to draw generalities from the data (such as plankton assemblages among a broad range of Raymont, 1980; Smayda, 1980). It is, of course, pelagic systems, in the sea and among inland attractive to turn to the latter publications and waters, seeking to identify general patterns and to précis and paraphrase the accounts. It may common behaviour. In the second main section seem that this is the option that has been fol- (7.3), the processes that govern the assembly lowed but the present account is closer to the of communities and shape their structures are intentions of Margalef (1967)inbeing ordered traced in detail. Because some of the terminology more about the main habitat constraints. This has been used uncritically in the literature, some- permits its emphasis to be directed to the struc- times erroneously and often confusingly, their tural elements of the organisation of marine usage in the current work is explained in a sep- phytoplankton. In no sense does it provide either arate text (Box 7.1). a catalogue of the species to be found in SPECIES COMPOSITION AND TEMPORAL CHANGE 303

Box 7.1 Working deﬁnitions of some terms used in community and ecosystem ecology

Niche The preferred use of this term refers to exploitable resources requiring particular organismic abilities or adaptations for their utilisation. In an evolutionary context, these abilities may be acquired by some species (who may become specialist in retrieving this part of the resource pool) and, perhaps to the extent that they do so better than others, whom they may eventually exclude through competition. With sufficient division of the resource pool (niche differentiation), however, many species are able to coexist in the same assemblage (see Tokeshi, 1997). More generalist species that may broadly share the same spectrum of resources (wide niche) constitute a guild or functional group. They may also coexist, until the resource diminishes to constraining proportions and becomes the subject of competition and potential exclusion of all but the superior competitor (Hardin, 1960). Power Poweriswork per unit time. The usual unit is the watt (W = Js−1). In the context of power delivery of primary production to the pelagic food web, it is more convenient to express power in units of kJ a−1. Salomonsen’s (1992) calculations of the volume-specific primary production in the plankton is typically within the range 100–1000 of kJ m−3 a−1. Emergy Emergy is the total amount of energy invested directly or available indirectly to a system but not all of which can deliver ecologically significant power (Odum, 1986). Odum (1988)went on to compare the transformity of the energy sources to the power yield as a ratio. This ranges from up to 1 (for PAR), through wind energy (623) and hydropower (23 500) to proteinacecus foods (1 to 4 million). Exergy Exergy is defined as the maximum flux of short-wave energy that a system can hold in the form of entropy-free chemical bonds, pending its eventual dissipation as heat (Mejer and Jørgensen, 1979). Exergy represents the information stored in the structure of the system and its ability to increase (Salomonsen, 1992). It may bolster the system against structural change when its maintenance becomes more energetically costly than its return in energy harvesting (see p. 376). Ascendency In the context of accumulating ecosystems, this is the quantifiable synthesis of growth, development and organisation of an ecosystem. System growth is defined as the increase in total system throughput and development as the increase in information of the network of flow structures (Ulanowicz, 1986). Thus, ascendency is a measure of the structure of an ecosystem based upon the degree of organisation (information) and functioning (system activity) (Kutsch et al., 2001). Succession. Here, usage is restricted to autogenic assembly processes that result in the substitution of species, usually in a recognisable series. The process is partly the consequence of changes to the environmental conditions wrought by the activities of earlier-establishing organisms, to the extent that they become more amenable to the later establishing of individuals of other species and less so the earlier species already established (see p. 359). Successions may culminate in a dynamic steady state, known as climax, where one species dominates overwhelmingly. The competitively best-fit species survives at the 304 COMMUNITY ASSEMBLY IN THE PLANKTON

expense of its rivals but there is little predictable about the sequence of species participating in the succession itself. Succession is now regarded as no more than a probabilistic sequence of species replacements in a weakly variable environment. Stability Stability is the tendency of the species composition of a community not to vary over a given significant period of time (Pielou, 1974). Observable stability carries different connotations according to context; it is better to refer to individual classes of stability by their own names (Lampert and Sommer, 1993): constancy, resistance and resilience. Constancy Only minor fluctuations in the number of species, individuals and aggregate biomass occur. The absence of change does not distinguish whether the environment is itself is also relatively constant, or whether the structure accommodates and survives forcing by external variations. Constancy is also used in the context of cyclical consistency and the return to precisely similar community structures (see p. 381). Resistance Resistance is the term for the situation in which despite external forcing, internal structure is preserved. This may be relative (weak forcing, resistant structure) or the forcing does not alter the current environmental constraint (see p. 376). Resilience (elasticity) Resilience describes the situation where environmental forcing causes a deviation in structure but the system returns (‘reverts’: Reynolds, 1980a)toits original condition. Resilience leads to constancy over a long period (Lampert and Sommer, 1993). Disturbance Disturbance is the situation in which the environmental forcing results in a significant shift from the original structure which is not recovered in the short term. Disturbance is a community response to the forcing. It should not be applied to the forcing (see pp. 372–9).

particular parts of the sea or an inventory of past Phytoplankton of the North Pacific surveys. Subtropical Gyre From the timeoftheearliest comparative The deep-water oceanic provinces of the Pacific, observations (e.g. those of Gran, 1912), system- Atlantic and Indian Oceans cover over half the atic differences in the abundance and composi- surface of the planet. Remote from the conti- tion of phytoplankton were recognised. At first, nental land masses, they are host to about one- it was supposed that these were due to differ- quarter of global net primary production. Within ential temperature and salinity preferences of these great basins, surface water movements con- thealgae. Gradually, however, floristic assem- stitute clockwise (in the northern hemisphere) or blages became associated with the extent and anticlockwise (southern hemisphere) geostrophic longevities of water masses in the major oceanic flows, or gyres (see Fig. 2.3). The North Pacific basins and their circulations (cf. Fig 2.3), sub- Subtropical Gyre, occupying an elliptical area ject to the modifying effects of adjacent shelf of some 20 million km2 located between lati- areas and coasts, and of such local aberrations tudes 15◦ Nand35◦ Nand between longitudes as upwellings, coastal currents and frontal activ- 135◦ Eand135◦ W, is the largest of these cir- ity. Some examples of the floristic distinctions culation features. It is also the Earth’s largest among these zones are noted below, with com- contiguous biome (Karl et al., 2002). The circu- ments on their environmental characters, con- lation substantially maintains a coherent mass straints, fertility and variability. of water and separates it from adjacent habitats. SPECIES COMPOSITION AND TEMPORAL CHANGE 305

Even the permanent pycnocline, located at a tripos)normally make up only a small part of the depth between 200 m and 1 km, isolates the sur- plankton. face waters from the deep, nutrient-rich layers The variability revealed by the ALOHA obser- beyond. As with the other major oceanic gyres, vations occurs on several timescales. Day-to-day the severenutrient deficiencies and low support- differences in primary production relate to dif- ive capacities of the surface waters of the North ferences in PAR income, especially that available Pacific have long been appreciated (TN < 3 µM, TP to the deep chlorophyll maximum. There are < 0.3 µM, SRSi < 20 µM: Sverdrup et al., 1942). On broad seasonal variations in primary production the other hand, the water has a high clarity (εmin rates(slightly higher in the northern-hemisphere ∼0.1 m−1:Tyler and Smith, 1970,quoted by Kirk, summer) and biomass (slightly higher in the 1994). Its low planktic biomass and weak areal winter). However, these oscillations are also sub- production have also been accepted (Doty, 1961; ject to larger fluctuations on supra-annual or Beers et al., 1982;Haywardet al., 1983). The sup- aperiodic scales (chlorophyll range over the full posed constancy of these conditions nurtured an study period, 13–36 mg chla m−2). Longer peri- idea that the system had achieved the steady state ods of weak winds and enhanced stability, in of a successional climax (Venrick, 1995). There 1989, were followed by blooms of the nitrogen- is certainly little doubt that the North Pacific fixing Cyanobacterium Trichodesmium. During Subtropical Gyre is a feature of great antiquity March–April 1997, nutrient upwelling, caused by whose properties and boundaries have persisted astrongwinddivergence, was followed by a since the Pliocene period (10 Ma B.P: Karl et al., significant bloom of Rhizosolenia styliformis. Like 2002). Hemiaulus (Heinbokel, 1986)this diatom is also Since the establishment in 1988 of a monthly able to supplement its supply of fixed nitro- monitoring programme of the biomass and pro- gen which, in this instance, is provided by an ductivity of the phytoplankton in North Pacific endosynbiotic Cyanobacterium, Richiella. Subtropical Gyre, at a station near Hawaii called These fluctuations are caused proximally by ALOHA, a much clearer picture of its community events that either increase the nutrient resource dynamics has become available (Karl, 1999;Karlet or decrease the mixed depth. In turn, these al., 2002). This confirms the low depth-integrated follow the supra-annual ‘El Niño’ oscillations phytoplankton biomass (averaging 22.5 mg chla in wind forcing and gyre circulation brought m−2; concentrations typically increase from < 0.2 about by high water temperatures in the west- mg chla m−3 near the surface to a typical deep ern Pacific. As these events subside, vertical mix- chlorophyll maximum at between 80 and 120 m ing in the gyre weakens, there is a decreased depth of up to ∼0.8 mg chla m−3)andlow pri- nutrient flux from depth and the upper waters mary production rates (484 mg C m−2 d−1. S.D. become more oligotrophic. Dominance reverts to ± 129). However, these data reveal more variabil- picocyanobacteria and nanophytoplankton and, ity than might be expected of a fully equilibrated potentially, to nitrogen-fixing bacteria. Annual steady state. carbon fixation settles back to ∼160gCm−2 The floristic composition also proved to be sur- a−1 which is consumed mainly in turning over prising. Whereas the earlier published accounts amicrobial food web. focused on the dinoflagellates and diatoms, This pattern comprises what are mani- much the most abundant phototrophs and the festly the organisms best suited to the rar- largest fraction of the standing biomass are efied resources. Significant sedimentary losses prokaryotes, especially Prochlorococcus (some 50%) are obviated, except during episodes of diatom and smaller amounts of Synechococcus.Lesser num- abundance (Karl, 1999). The point to emphasise bers of eukaryote haptophyte (Umbellosphaera)and is that although the biomass remains generally chrysophyte (Pelagomonas)nanoplankters (Letelier very resource-constrained, it is not in an unmov- et al., 1993;Campbell et al., 1994)arepresent. The able steady state and the events to which it is diatoms (species of Rhizosolenia, Hemiaulus)and susceptible influence the rate and direction of dinoflagellates (Prorocentrum, Pyrocystis, Ceratium change in community composition and function. 306 COMMUNITY ASSEMBLY IN THE PLANKTON

Phytoplankton of other low-latitude gyres Pacific and Atlantic Oceans, whereas Antarctica Few other modern ocean surveys match the com- is wholly surrounded by an almost continuous prehensiveness of the ALOHA series but more lim- Southern Ocean which interfaces with the South ited datasets suggest a common organisation. In Atlantic, the Indian and the southern Pacific. the South Pacific Gyre, DiTullio et al.(2003)found In the Arctic Basin, seasonal dynamics are picoplanktic Cyanobacteria to be major compo- supposed to be dominated by changes in day nents of the assemblage, Prochlorococcus dominat- length and radiation intensity. There are few ing over the scant biomass of Synechococcus and seasonal studies from which to gauge succes- other eukaryotic plankters that included Phaeocys- sional changes (Smayda, 1980). In the winter, tis and prasinophytes as significant constituents. underwater light availability is severely con- Prochlorococcus is abundant in the low-biomass straining in both ice-covered and ice-free areas region of the central Indian Ocean (between 5◦ N and phytoplankton biomass is low. While there and 30◦ Sand55◦ and 100◦ E; < 0.1 mg chla m−3) is little evidence of much seasonal growth where Trichodesmium is also common. Coccol- under permanent ice, lengthening days bring ithophorid nanoplankton, diatoms and dinoflag- significant increases in standing crop in ice- ellates contribute to modest seasonal biomass free areas (Smayda, 1980). Generally, diatoms are increases during May and June, in the wake overwhelmingly dominant, with biomass being of the monsoon period (various entries in Ray- shared among a relatively small number of main mont, 1980). In the North Atlantic Tropical Gyre, species (Achnanthes taeniatum, Chaetoceros diadema, picoplanktic communities supporting fully devel- Corethron criophilum, Skeletonema costatum, Coscin- oped microbial food webs have been demon- odiscus subbulliens, Rhizosolenia styliformis and Rhi- strated byFinenko et al.(2003). The dominant zosolenia hebetata). Phaeocystis sp. isoneofthefew primary producers in the Sargasso Sea (part of non-diatoms that can be plentiful in summer; the adjacent subtropical gyre) are Prochlorococcus, three species of Ceratium (C. longipes, C. fusus and again being most abundant in a deep (∼75 m) C. arcticum), three of Peridinium (P. depressum, P. maximum (Moore et al., 1998). Previous investi- oratum and P. pallidum)and the prasinophyte gations of the seasonality of microphytoplank- Halosphaera are also noted. ton seasonality of the Sargasso Sea (Riley, 1957; In intermediate zones, where the ice cover Hulburt et al., 1960;Smayda, 1980)recognised may be broken but its melting proceeds through that the limited abundance of spring diatoms much of the short summer, density differences (Rhizosolenia, Chaetoceros spp.) gives way to a long contribute to a substantially reduced mixing period of relative abundance of nanoplanktic depth. Within such polynia,theremay be a char- Umbellosphaera and other coccolithophorids, and acteristically strong seasonal development of phy- to Trichodesmium and ceratians such as Ornithocer- toplankton. Green flagellates may appear under cus during summer. the thinning ice pack, to be followed by such diatoms as Achnanthes and Fragilariopsis species Phytoplankton of high latitudes through the period of ice-break. These may per- Towards the edgesofthegreatoceanic provinces, sist until new ice is formed towards the end of altered environmental conditions (mostly related summer (perhaps as little as 2–4 months later) to the proximity to land masses: depth, light and, but are often joined by other diatoms (Chaetoceros, especially, elevated nutrient availability) support Thalassionira spp.), Phaeocystis and Ceratium species, alternative assemblages. In addition, the ten- together forming a distinctive species assemblage dency towards the polar regions is to weaker (Smayda 1980). and more seasonal thermal stratification. How- ever, there are further contrasts between the cir- Phytoplankton of deep boreal waters culatory patterns of the northern and southern The Atlantic to the north of the North Atlantic hemispheres that relate to the distribution of Drift Current, together with its arms to the land masses. The physical structure of the north- Labrador and Norwegian Seas (roughly, the open ern high latitudes is separable between the Arc- ocean to the north of a line from 35◦ N, 75◦ Wand tic Polar Basin and the boreal reaches of the 45◦ N, 10◦ W) and the Pacific Ocean to the north SPECIES COMPOSITION AND TEMPORAL CHANGE 307 of the Kuroshio Current (roughly, from 35◦ N, nitzschioides becoming increasingly prominent 145◦ Eto55◦ N, 145◦ W) constitute the two main towardsthe late summer. Dinoflagellates are also boreal oceanic provinces. The Continuous Plank- conspicuous in the summer months, especially ton Recorder (CPR), devised originally by Sir Alis- Exuviaella spp., several Peridinium spp., ceratian ter Hardy (1939)toinvestigate mesoscale patch- spp. (Ceratium longipes, C. fusus, C. furca and C. iness, was used extensively and over a number tripos). Gymnodinioids are common throughout of years to reveal microphytoplanktic structure theMay to November vegetation period (synthe- in the boreal North Atlantic Ocean (Colebrook et sis ofSmayda, 1980,based on the observations al., 1961;Robinson, 1961, 1965). These identified of Halldal, 1953). the ceratians C. carriense, C. azoricum, C. hexacan- In the North Pacific, a mainly sub-Arctic cold- thum and C. arcticum and the diatom Rhizosolenia water community occupies the boreal waters sep- alata as being primarily oceanic species, quoted arated from the Central Pacific by the warm in a sequence from warmer southerly water to Kuroshio Current (Marumo, in Raymont, 1980). the colder northern masses. Many other species The biomass supported is contrasted with the found were adjudged to have originated in adja- meagre populations of the gyres to the south. cent shelf waters (e.g. Ceratium lineatum, Thalassio- Typically, diatoms (species of Chaetoceros, Corethron thrix longissima, Nitzschia spp.), yet others to have and Fragilariopsis, Rhizosolenia hebetata, Thalas- amore general occurrence (Thalassionema nitzschi- sionema nitzschioides, Thalassiosira nordenskioeldii) oides, Rhizosolenia styliformis, R. hebetata). Phyto- dominated the spring–summer maxima. Sum- plankton abundance increases with increasing mer dinoflagellates included Ceratium fusus. day length, to a typical maximum of ∼2mg chla m−3 in May or June. Among many species Phytoplankton of the Southern Ocean present, diatoms (Thalassiosira, Thalassionema and Adiscrete ‘Southern Ocean’ was distinguished Rhizosolenia)generally dominate. In summer, Cer- from its contiguous oceans (Atlantic, Indian and atium fusus, C. furca and C. tripos are relatively com- Pacific) after its effective isolation by a series mon. of circumpolar fronts (see below) was first fully Smayda (1980)reviewedHolmes’s (1956)recon- appreciated (Deacon, 1982). The key subtropi- struction of algal periodicity in the Labrador Sea. cal frontal system stretches around the entire Many species are common to the CPR listings Antarctic continent, generally between the lati- for the open Atlantic, with species of Thalassiosira tudes 40 and 50◦ S, uninterrupted but for the pen- and Thalassionema prominent, along with several etration of the Patagonian region of South Amer- species derived from adjacent shelfs and coasts ica. The area enclosed represents almost 20% of (notably species of Chaetoceros, Coscinodiscus, Fragi- the planetary ocean surface and it is now known lariopsis)orfromtheArctic(Ceratium arcticum and to play an important role in regulating the plan- Peridinium depressum). Diatoms (especially Fragilar- etary climate (Boyd, 2002). Variations in the syn- iopsis nana, Fragilaria oceanica, Rhizosolenia hebetata, thesis of the DMSP precursor (see Section 4.6.2), Pseudonitzschia delicatissima) dominated the single the turnover of macronutrients and the passage late spring/early summer maximum. Dinoflag- of photosynthetically fixed carbon to Antarctic ellates, including Peridinium depressum,wererel- heterotrophs are all mediated by the phytoplank- atively common in summer. Coccolithophorids, ton. Over geological time, the carbon exchanges especially Emiliana huxleyi,arealso numerous in of the Southern Ocean have impinged signifi- the North Atlantic Ocean during summer, in cantly on planetary climate. some years producing significant blooms (Balch Within the ocean, frontal systems separate et al., 1996). approximately concentric inner water masses, In the Norwegian Sea, the sequence of dom- each having distinct physical and chemical iden- inance moves from diatoms (initially Chaetoceros tifiers. The seasonal advance and retreat of sea spp., Fragilariopsis nana in the late spring), with ice cover adds to the physical complexity of Chaetoceros convolutus, Corethron hystrix, Thalas- the Southern Ocean, defining permanently open- siothrix, Rhizosolenia hebetata, R. styliformis, ocean and seasonally ice-covered zones (POOZ, Pseudonitzschia delicatissima and Thalassionema SIZ). However, a general property of all the 308 COMMUNITY ASSEMBLY IN THE PLANKTON

substructures is the degree of environmental con- interface with the land masses, or with the control of phytoplankton that they exert. In short, tinental shelves of which they are part, or with chlorophyll concentrations (generally <0.3 mg the margins of another oceanic province. Each chla m−3)areratherlowerthan the perennial interface creates distinctive physical environ- capacity of the macronutrients to support (up ments for phytoplankton growth and selection. to 15 µMDIN,upto2µMBAP).The condi- Fronts at the mutual interface of two oceanic tion, now referred to as HNLC (for high nitro- masses persist because differences in their tem- gen, low chlorophyll: Chisholm and Morel, 1991), perature and salinity (and, hence, density) resist is attributable to several constraints (the interac- intermixing. The most significant fronts sepa- tion of daily irradiance, vertical attenuation and rate thepermanently stratified tropical oceans mixed-layer depth; silica exhaustion; grazer con- from the cold, well-mixed waters of the polar trol) but experiments (such as IRONEX, SOIREE: seas, and which, roughly, are located at around see Section 4.5.2)haveshown iron deficiency to 40◦ Nand40◦ S. The polar convergences are well be often the critical factor (for a full review, defined, especially in the Pacific, by sharp gradi- see Boyd, 2002). With ambient TFe levels <10−9 ents of surface temperature that correspond to M, the short ‘window of blooming opportunity’ thearea in which the denser cold water is slid- allowed by the austral summer sustains only ing under the lighter warm surface flow. A few modest phytoplankton growth before further degrees to the equatorial side of the polar front is recruitment becomes iron-limited. Even though a further, rather less abrupt subtropical conver- the severity and timing of the limitation may gence, formed between the warmer central por- vary among zones and the growth of diatoms tions of the gyre interface with the peripheral depletes the stock of dissolved silicon (data of geostrophic flow. Boyd et al., 1999), the ultimate controlling role of In both instances, the interfaces abound with iron is quite general across the Southern Ocean. instabilities and a degree of intermixing. Phy- The dominance of Antarctic waters by toplankton present in either water mass are diatoms was detected in the earliest plankton sur- confronted with altered environmental condi- veys (Gran, 1931;Hart, 1934). The major species tions, offering improved insolation to the polar include Chaetoceros neglectus, C. atlanticus, Corethron assemblage and, perhaps, more nutrient to the criophilum and species of Fragilariopsis, Nitzschia species in the subtropical water. In a transect and Rhizosolenia (which include R. alata and R. across the South Pacific Ocean, following longi- hebetata). In the seasonally ice-covered zones, tude 170◦ Wfrom the Antarctic continent to the Chaetoceros neglectus and Nitzschia closterium are Equator encountered its highest chlorophyll con- abundant close to the receding ice edges, before centrations (>0.5 mg chla m−3)inthe vicinity giving place to the summer assemblage. The hap- of the polar and subtropical fronts (DiTullio et tophyte Phaeocystis antarctica also blooms in some al., 2003). In the latter instance, there was a dis- parts of the Southern Ocean. It benefits from tinct subsurface maximum at a depth of about modest iron enrichment (as do other species) but 40 m. Between the fronts, the dominant phyto- its growth does not run into silicon limitation plankters were coccolithophorids, chrysophytes and it is also more efficient in adapting to vari- and Pelagomonas;prasinophytes, cryptophytes and able light and carbon deployment (Arrigo et al., Phaeocystis also contributed to the standing crop. 1999). The abundance of the prymnesiophyte flag- Diatoms were scarce on this occasion (the silicon ellate Pyramimonas is also sensitive to light and concentrations were <1 µM) but other authors iron levels (M. van Leeuwe, quoted by Boyd, 2002). have found the Polar Front to be the main loca- However, picoplanktic prokaryotes become relation of Antarctic diatom blooms (Smetacek et al., tively more scarce with increasing latitude (Det- 1997). mer and Bathmann, 1997). Upwellings Oceanic fronts The major upwellings occur along continental The margins of each of the major circulatory seaboards, where the circulation current and provinces so far considered in this section can the prevailing wind have the same direction. SPECIES COMPOSITION AND TEMPORAL CHANGE 309

The Coriolis forces acting on the flow tends to theBenguela upwelling, where Chaetoceros species drag surface water away from the coast (Ekman are similarly dominant and where primary pro- transport), thus entraining deeper (usually from duction rates of 0.5–2.5 g C m−2 d−1 have been below the pycnocline) to the ocean surface, where reported (Steemann Nielsen and Jensen, 1957). it ‘upwells’ a short distance from the shore. This Off California, the most common phytoplank- waterisgenerally cold but relatively nutrient- ton during intense upwelling included Rhizosole- rich and, entering the photic zone, becomes sup- nia stolterforthii, Skeletonema costatum and Lepto- portive of high biological production and prized cylindricus danicus (Eppley, 1970). The recent time fisheries. For example, the Canaries Current – the series of Romero et al.(2002)ontheupwelling south-flowing arm of the North Atlantic Subtrop- fluxes in the region of Cap Blanc, north-west ical Gyre – coincides with the North-East Trade Africa, distinguished periods when character- Wind along the coastline of Mauritania and Sene- istically oceanic diatoms (Nitzschia bicapitata, gal. The matching structure in the North Pacific, Thalassionema nitzschioides, Fragilariopsis doliolus) the California Current, is also responsible for were dominant from those when near-shore San Francisco’s legendary fogs. Yet more strik- species were ascendant (including Cyclotella ing are the Benguela and Peru Currents, respec- litoralis, Coscinodiscus and Actinocyclus spp.). tively moving up the west coasts of Africa and During relaxations, production falls, diatom South America, enhancing biological production dominance fades as cells are lost by sink- in their wakes (to >400gCm−2 a−1;seeBehren- ing and decay, and smaller or motile algae field et al., 2002) and especially where they divert assume relative importance. Coccolithophorids from the coast lines (again respectively) near (Umbellosphaera) and small dinoflagellates (Lingulo- Gabon and the Galapagos´ Islands. dinium polyedrum, Gymnodinium catenatum, both The intensity of upwelling is not continu- notable as harmful bloom species) mark the ous, fluctuating with seasonal variations in wind transition to calmer, nutrient-depleting condi- strength and provenance. In the Indian Ocean, tions (Smayda, 2002). With falling fertility at upwellings in the Arabian and Andaman Seas are the surface, chlorophyll maxima develop at strongly seasonal, being related to the monsoonal depth and in which other coccolithophorids (e.g., episodes. The El Niño oscillations alternate sup- Florisphaera spp.: Raymont, 1980)and dinoflag- pression and enhancement of the strength of ellates (notably Dinophysis spp.: Reguera et al., upwelling of the Peru Current. When coastal 1995)may become relatively abundant (Raymont, winds weaken and the sea surface calms, the mix- 1980). ing of the water also becomes less intense and warm, nutrient-poor water persists at the surface. Shelf phytoplankton This phenomenon is known as ‘post-upwelling What are recognised as the terrestrial land relaxation’. masses are blocks of continental crust that, in Both the upwellings and the relaxations cre- geological time, are moved apart or are coalesced ate distinctive environmental conditions for phy- by the tectonics of the plates of oceanic crust. toplankton development. Guillen et al.(1971) Whereas the active formative ridges and the deep refer to the periods of high primary produc- subduction trenches power the changing position in the coastal Peru Current (0.3–1.0 g C tions of the continental masses, the gaps between m−2 d−1), nurtured by macronutrient levels them are water-filled. In fact they are the reposi- shown byotherstobeupto2µMPand 20 tory of 97% of the planetary total. At the present µMNandsupporting phytoplankton biomass time and, subject to fluctuation of ±50 m due to equivalent to the order of 2 mg chla m−3. thechanges in the volume stored as polar ice, for Diatoms (especially Rhizosolenia delicatula, Thalas- most of the last 250 million years, the low-lying siosira subtilis, Skeletonema costatum and Chaeto- continental perimeters have been inundated by ceros debilis) dominated the flora, species of the sea,toadepth of ≤200 m. Collectively, these other groups of organisms (dinoflagellates, coc- are the continental shelves. Grading at first gen- colithophorids) making up only a small percent- tly away from the coastline, the shelf extends to age of the biomass. Similar conditions obtain in the true continental edge, the abrupt, steep slope 310 COMMUNITY ASSEMBLY IN THE PLANKTON

to the ocean floor, >2km(and locally up to 6 km) development of a May diatom bloom (typical beneath the water surface. maximum 2–3 mg chla m−3), generally featuring The width of the continental shelves varies Thalassionema nitzschioides, Rhizosolenia hebetata, R. with location, literally from a few kilometres delicatula, Chaetoceros and Thalassiosira species. In (as along the coast of central Chile, of north- thesummer, dinoflagellates are relatively much east Brasil and the south-eastern seaboard of Aus- more abundant, especially Ceratium fusus, C. furca tralia) to the great expanses that characterise and C. tripos; Heterocapsa triquetra, Karenia mikimo- theSea of Okhotsk, the East China Sea, the Ara- toi and Dinophysis acuminata also feature. Rhizosole- fura Sea, the Gulf of Maine, the Grand Banks nia alata and R. styliformis are most common in of Newfoundland and the seaboards of north- autumn (various sources, compiled by Raymont, west Europe (the Baltic Sea, the North Sea and 1980). theEnglish Channel). Though mutually very dif- The Sea of Okhotsk is generally partly or ferent from each other in their oceanic inter- wholly ice covered in winter and the onset of the faces, latitude, temperature and fluvial influence, spring bloom (of diatoms Chaetoceros spp., Rhizo- they share common attributes of close mechani- solenia hebetata, Thallasionema nitzschioides, Thalas- cal coupling to the adjacent littoral and/or ben- siosira nordenskioeldii and Leptocylindrus danicus)is thic habitats through wind and tidal mixing. quite abrupt. The production and phosphorus Even so, the dilution of underwater light by mix- dynamics of these episodes have been the sub- ing in shallow areas is generally less extreme ject of recent investigations by Sorokin (2002)and than in the oceanic areas beyond. Coastal shelf Sorokin and Sorokin (2002). waters are, indeed, distinctive from the ocean in supporting alternative planktic comunities Coastal and near-shore waters under distinctly differing environmental condi- Near-shore shelf waters may be further distin- tions (Smayda, 1980). guished by the potential to support greater lev- Smayda (1980)developedhisoverviewofphy- els of biomass, production and diversity, and toplankton succession in open shelf water based with more variability of abundance and domi- on well-studied examples from the Gulf of Maine nance. Shallower water, experiencing more rapid and the North Sea. The phytoplankton of the Gulf interchange of resources with the bottom sedi- of Maine, located between 41◦ and 44◦ N, is char- ment, together with the inflow of ‘new’ resources acterised by the development, commencing in from the land, provide more growth opportuni- March or April, of a spring diatom bloom, usu- ties and more support to accumulating biomass. ally dominated by Thalassiosira nordenskioeldii with The phytoplankton that can be supported may Porosira glacialis and Chaetoceros diadema.Aswater be regarded as a more productive sub-set of the temperatures warm, other species of Chaetoceros adjacent shelf-water assemblage but some species (notably C. debilis)becomerelatively more abun- may benefit or express advantage more than oth- dant, before yet others (including C. compressum) ers and there may be additional species that are take over dominance in early summer. Diversity rare or absent further off shore. is further and variably increased by the rela- The relative logistic ease of sampling coastal tive abundance of dinoflagellates (ceratians Cer- waters also makes for the assembly of more atium longipes, C. tripos, C. fusus and peridinians detailed time series, although, as Smayda (1980) Peridinium faroense, Heterocapsa triquetra, Scrippsiella reminded us, the sequence of species abundances trochoidea)and coccolithophorids (especially Emil- are not necessarily successional. Rather, these iana huxleyi). During the autumn, diatom domi- are temporal sequences of effects that may be nance isrestoredbyRhizosolenia species (R. alata, under physical (wind, weather, offshore current) R. styliformis, R. hebetata, a.o.) and Coscinodiscus control or, at best, the results of successional species. events generated elsewhere. Smayda’s (1980)own In the shelf waters around the British Isles, data from Naragansett Bay, Rhode Island, USA, the influence of penetrating Atlantic water is reveal an initial spring flowering of the dominant variable but it fails to suppress the indigenous shelf water diatom, Thalassiosira nordenskioeldii, SPECIES COMPOSITION AND TEMPORAL CHANGE 311 though this is under way at least a month ear- peridinian (especially Scrippsiella trochoidea), pro- lier than it is offshore. Later common diatoms rocentroid and ceratian (Ceratium furca, C. fusus included Skeletonema costatum, Asterionella japonica and C. tripos) dinoflagellates. As seas slacken and and the large-celled Cerataulina pelagica.Inthe nutrients weaken, ‘Stage 2’ blends into ‘Stage English Channel, there is a variable influence 3’, the genera Bacteriastrum, Corethron and large of Atlantic water supporting dominant Thalas- species of Rhizosolenia (e.g. R. styliformis)become sionema or Thalassiosira populations but it is gen- themain diatoms, while dinoflagellates of the erally masked by indigenous developments of genera Ceratium, Dinophysis, Gymnodinium,and diatoms and dinoflagellates (Chaetoceros compres- Lingulodinium may increase, along with coccol- sus, Rhizosolenia delicatula, Heterocapsa triquetrum, ithophorids such as Emiliana.Byhigh summer Karenia mikimotoi, Prorocentrum balticum)inearly and the onset of ‘Stage 4’, the ria is substantially summer and of ceratians (Ceratium fusus, C. tri- stratified and nutrients in the surface waters pos)inmidtolatesummer (Holligan and Har- are severely depleted. Only the large Rhizosolenia bour, 1977). Typical maximum chlorophyll con- species (they may include R. calcar-avis) and Hemi- centrations were in the range 3–4 mg chla m−3. aulus hauckii persist in a plankton otherwise dom- At the regular sampling station used by Harbour inated by Ceratium, Peridinium and Prorocentrum and Holligan (depth ∼70 m), areal biomass gen- species. Alternatively, nitrogen-fixing Cyanobac- erally varied between ∼20 mg chla m−2 in winter teria may appear at this time. It is noteworthy and ∼150 mgm−2 during the April bloom period. that all these species have rather low surface- However, a feature of these enriched near-shore to-volume ratios (sv−1 ≥0.3) and the populations areas is the appearance in calmer weather of are mostly small (∼10 mL−1). In enriched coastal the haptophyte Phaeocystis and occasionally abun- waters, prolonged stratification may instead pro- dant growths of such nanoplankters as Carteria, ceed from ‘Stage 3’ in which the smaller ‘red-tide’ Dunaliella or Nannochloris. dinoflagellates (including Alexandrium tamarense) One of the most significant and seminal persist and continue to grow into substantial studies of near-shore marine phytoplankton was nuisance populations (see also Section 8.3.2). maintained by Ramon´ Margalef over a num- Autumn cooling and renewed mixing restores the ber of years on the Ria de Vigo in north-west plankton back to ‘Stage 1’. Spain. He incorporated his findings into a devel- Margalef’s descriptions provide a basis for opment of a general explanation of the mecha- comparison with those of Smayda (1980)refer- nisms of seasonal change in community struc- ring to the inshore waters of Norway’s fjord coast- ture (Margalef, 1958, 1963, 1967). Although influ- line. Although some 25◦–30◦ of latitude further enced by later observations made in the Mediter- north and experiencing lower summer temper- ranean Sea, Margalef recognised four distinct atures, the sequences of phytoplankton domi- stages of the development. Early in the northern- nance have many similarities to those of Spain’s hemisphere year, when coastal waters are still rias. In Ullsfjord (71◦ N), an April diatom bloom- cool, well-mixed (he called them ‘turbulent’) and ing of Chaetoceros species, Fragilaria oceanica, Tha- relatively charged with nutrients, small-celled lassiosira decipiens and T. hyalina is followed by diatoms (Skeletonema costatum, Leptocylindrus dani- a July–August bloom featuring Chaetoceros debilis, cus, Chaetoceros socialis, C. radicans, Rhizosolenia alata Pseudonitzschia delicatissima, Skeletonema costatum, and R. delicatula)predominate, with small flagel- Thalassiosira nordenskioeldii, Leptocylindrus danicus lates (Eutreptia, Platymonas, Rhodomonas a.o.), occur and Rhizosolenia alata.Dinoflgellates are also during this ‘Stage 1’. All these algae have high present in summer (see below) but they are much surface-to-volume ratios (sv−1 ≥1), are capable less abundant than diatoms. In Trondheimsfjord of rapid growth at low temperatures and form (64◦ N), blooming starts in March, with Fragilar- populations of between 102 and 103 cells mL−1. iopsis cylindrus, Porosira glacialis, Skeletonema costa- ‘Stage 2’ tends tobedominated by a more mixed tum, Thalassiosira hyalina and several other species, community of larger-celled diatoms Chaetoceros then continues through to May/June (with Chaeto- species, Lauderia annulata, Eucampia cornuta)and ceros debilis, Leptocylindrus danicus, Pseudonitzschia 312 COMMUNITY ASSEMBLY IN THE PLANKTON

delicatissima, Skeletonema costatum and Thalas- large crops of this alga had been observed previ- sionema nitzschioides prominent). Cerataulina pelag- ously and have been since but the 1988 event was ica, Eucampia zodiacus and Rhizosolenia fragilissima startling in its magnitude. The general eutroph- are summer species. Dinoflagellates, including ication of the Danish coastal waters was blamed Exuviaella baltica, Heterocapsa triquetra and Scripps- but the proximal cause was the combination iella trochoideum and ceratians, approximately in of a strong outflow from the Baltic with calm the sequence Ceratium longipes, C. tripos, C. fusus, and sunny weather in the Kattegat, favouring develop in summer but rather more strongly shallow stratification and the growth of oppor- than they do further north. tunist motile algae – in this case Chrysochromulina In the Oslofjord (59◦ N), Skeletonema is the (Edvardsen and Paasche, 1998). most important diatom during the March Extending eastwards from the Kattegat and bloom, with increasing representation by Thalas- theØresund, the Baltic Sea is a substantially siosira nordenskioeldii,various Chaetoceros species landlocked shallow sea. It is characterised by the (C. debilis, C. socialis,thenC. compressus), Rhizo- dilution of its salt content by an excess of pre- solenia alata and Pseudonitzschia delicatissima.By cipitation over evaporation, and by some large summer, Lauderia borealis, Cerataulina bergonii, river inflow discharges. Whilst the structure of Cyclotella caspia and Chaetoceros species are promi- theplankton varies with the salinity gradient nent, together with Phaeocystis pouchetti and a across the Baltic, the tendency of warm fresh sequence of dinoflagellates (Scrippsiella, Hetero- watertofloat on the colder, salt water emphasises capsa and Prorocentrum micans, and ceratians Cer- thevertical stability and minimises the horizon- atium longipes, C. tripos and C. fusus). In the inner tal gradient in the summer. West of the constric- fjord, many species of nanoplanktic flagellates tion between Denmark and Sweden, this effect is are recorded, among which Micromonas, Eutrep- normally overwhelmed by tidal and wind mixing tia, Cryptomonas, Rhodomonas, Ochromonas, Pseudo- but, as mentioned above, there have been excep- pedinella and Chrysochromulina can be abundant. tions with dramatic results. Within the Baltic Coccolithophorids (Emiliana, Calciopappus, Anthos- and its two arms, the Gulfs of Bothnia and Fin- phaera)arealsonumerous in the outer fjord at land, the sequences of phytoplankton dominance this time. Inrecentyears,Alexandrium and other differ from those on the west side of Scandinavia. red-tide species have tended to be abundant in The sea being usually ice-covered in winter, the thelocality. In the autumn, diatom dominance first growths of the year may be small flagellates (Skeletonema, Leptocylindrus)isre-established. (e.g. Chlamydomonas, Cryptomonas) beneath the ice Alittle to the south, in the Kattegat, the surface. After the break-up of the ice, diatoms spring diatoms (Skeletonema costatum, Chaetoceros (including Achnanthes taeniata, Skeletonema costa- compressus, Rhizosolenia delicatula, Rhizosolenia alata tum and Thalassiosira baltica)generally dominate and Pseudonitzschia delicatissima)giveplaceto but with developing column stability, essentially Cerataulina and Leptocylindrus in the summer freshwater species of Oocystis, Monoraphidium a.o months, together with variable amounts of Phaeo- (Edler, 1979;Wasmund, 1994; Samuelsson et al., cystis pouchetti, Heterocapsa triquetrum, Karenia miki- 2002)and picocyanobacteria (Kuuppo et al., 2003) motoi, Prorocentrum minimum and Ceratium species. become established. However, it is the prominent In the spring (May–June) of 1988, Chrysochromu- cyanobacterial flora (Anabaena lemmermannii, Aph- lina polylepis,athithertominorcomponent of anizomenon flos-aquae and Nodularia spumigenea are the nanoplankton of Norwegian and Danish themost notable) that now most characterises coastal water, produced a significant and harmful theBaltic Sea plankton. Blooms of toxic species bloom. Although equivalent to ‘only’ (Edvardsen currently exercise the academics and responsible and Paasche, 1998)about 10–20% of the diatom authorities alike (Kuosa et al., 1997). The autumn chlorophyll, the concentration of 40–80 mg chla flora is dominated by large centric diatoms, m−2 proved toxic to local fish populations as well Coscinodiscus and Actinocyclus (Edler, 1979). as to a variety of molluscs, echinoderms ascidi- Strong stratification is a feature also of ans and cnidarians (Dahl et al., 1989). Unusually the Black Sea. It has suffered intensive SPECIES COMPOSITION AND TEMPORAL CHANGE 313 eutrophication from its main influent rivers be about double this, but only during summer. (Danube, Dnestr, Dnepr and Don) since the Areal concentrations >100 mg chla m−2 are sub- 1970s: it is relatively nutrient-rich and its deep stantially confined to continental shelf waters; water isseverlyanoxic in summer (Aubrey et al., standing crops equivalent to >200 mg chla m−2 1996). The dominant species in spring include are restricted to enriched near-shore habitats and diatoms (Chaetoceros curvisetus, Rhizosolenia calcar- coastal lagoons. avis)but dinoflagellates (Prorocentrum, Heterocapsa Why is the biomass so relatively low in triquetra, Scrippsiella trochoidea, Ceratium tripos, most places? Supposing the primary producers Ceratium fusum a.o.) form a major part of the of the plankton to be everywhere sharing their biomass, and to which Emiliana huxleyi can environments with heterotrophic bacteria and sometimes make the largest contribution (Eker phagotrophic zooplankton, top–down depletion et al., 1999;Eker-Develi and Kideys, 2003). During is a less likely generic explanation than is severe thesummer, diatoms become rare while coccol- bottom–up regulation by a poverty of nutrient ithophorids and red-tide dinoflagellates become resources and by an inadequacy of photosyn- dominant (Velikova et al., 1999). thetic energy, consequential upon deep mixing Another weakly flushed, river-enriched and the erratic dilution of the harvestable pho- coastal area of the Mediterranean is the north- ton flux. Only where an adequate supply of a full ern Adriatic Sea. Its main phytoplankton species spectrum of essential nutrients coincides with are diatoms (Chaetoceros, Rhizosolenia, Cyclotella high light income into a shallow, clear, mixed and Nitzschia spp. and dinoflagellates Prorocen- layer is there a carrying capacity sufficient to sup- trum and Protoperidinium:(Carlsson and Granéli, port potentially high producer mass. However, 1999). Finally, on the Tyrrhenian Sea (western) inadequacies in either restrict the carrying capac- coast of Italy, Sarno et al.(1993) compared the ity, by imposing limitations on the ability of algae phytoplankton of the Fusaro Lagoon with the to grow and divide. adjacent waters of the Golfo di Napoli. Here, Is one of these more important than the dinoflagellates (Prorocentrum micans)maintained a others? Nutrient poverty and light limitation large winter population but this was replaced by place quite different impositions on algal growth, aFebruary–March diatom bloom, dominated by while differences in tolerances and adaptations Skeletonema costatum, Chaetoceros socialis and other to survive extremes are instrumental in species species and by Cyclotella caspia. Alexandrium and selection. The effects can be represented graph- Dinophysis featured in the summer plankton as ically to demonstrate the interaction of these did a number of prasinophytes (e.g. Pyramimonas factors, both in terms of habitats and of the spp.) and euglenoids (Eutreptiella sp.). Chlorophyll attributes of the species for which they select. concentrations varied up to a maximum of ∼70 We may start with Margalef’s (1978)‘tentative’ mg chla m−3 at the surface, and to ∼50 mg m−3 plot to illustrate the sequence (he called it a atadepthof4m. ‘succession’, which usage will be discussed in Section 7.3.2)ofphytoplankton dominance in 7.2.2 Species assemblage patterns relation to nutrients and stratification (he used in the sea theterm ‘turbulence’). A simplified version is Several deductions emerge from the above excur- shown inFig.7.1. The original diagonal of his sion around the world’s seas and their repre- plot tracked the four developmental stages in sentative phytoplankton assemblages. One of the theRia de Vigo, progressing from the Stage-1 most self-evident of these is just how rarefied diatoms of the still well-mixed, nutrient-rich con- is the phytoplankton over much of the ocean. ditions of the early vegetative season, through For much ofthetropical ocean, the concentra- the Chaetoceros- and Rhizosolenia-dominated stages tion of primary-producer chlorophyll is generally to theStage-4 preponderance of dinoflagellates much lower than 1 mg chla m−3,andequiva- capable of exploiting the well-stratified and lent to little more than 20 mg chla m−2.Inthe resource-segregated water column to compensate temperate ocean, maximal concentrations may thenutrient exhaustion of the surface water. 314 COMMUNITY ASSEMBLY IN THE PLANKTON

Succession

Figure 7.1 Simplified version of Margalef’s diagram summarising seasonal change in phytoplankton composition in the sea as a direct function of weakening ‘turbulence’ and Figure 7.2 The ‘mandala’ (of Margalef et al., 1979), diminishing free nutrients. Redrawn with permission from developed from Fig. 7.1,relating seasonal change to Smayda and Reynolds (2001). environmental selection of life forms and life-history traits. L and T are standard dimensionless units of length and time. Redrawn with permission from Smayda and Reynolds (2001). Margalef (1978) contended that the progression moved from r-selected to K-selected species (see of life forms, rather than species, and a further p. 209). The ‘tentative’ element was the widening trajectory selecting for the smaller, rounded ‘red- of the representation to embrace more oceanic tide’ dinoflagellates. diatoms (Thalassiosira,atthetopright of the In an early attempt to apply Margalef’s (1978) successional diagonal), highly adapted dinoflag- conceptual model to freshwater phytoplankton, ellates (Ornithocercus at the bottom left) and to Reynolds (1980a) pointed to the frequent inci- insert coccolithophorids about half-way along. dence of nutrient-rich, low-mixing conditions Thus, the entire ocean flora was potentially expli- among shallow lakes. It was also recognised that cable through the relationship between mixing these conditions generally promoted the rapid and fertility. growth of small, exploitative organisms – in This was a remarkable and stimulating con- fact, precisely those with the classical attributes cept, relating evolutionary adaptations and sur- of r-strategists. Reynolds’ (1980a) view at that vival strategies to habitat factors. It is flawed, time was that, against the two major axes of in that to insert additional species from other Margalef’s model (Fig. 7.1), true r → K succession locations into a single r–K continuum breaks the would track more or less vertically. This means understanding of the succession. A more serious that the diagonal really relates only to mixing issue is the implication that nutrient availabil- intensity and consequential effects on nutrient ity and mixing are mutually correlated, whereas redistribution of nutrients and that the distin- they are independent variables. Margalef was guishing ability of the Thalassiosira–Chaetoceros clearly aware of these difficulties, for his original diatoms that were considered to be exclusively plot (Fig. 2 in Margalef, 1978)containsareference r-selected by Margalef needed a new classifica- to ‘red-tide’ dinoflagellates in the upper left-hand tion. Reynolds et al.(1983b)referredtothem as corner (‘high nutrients, low turbulence’), off the w-selected species, based on their morphologi- main successional diagonal. He noted their occur- cal and physiological adaptations to maintain rence as an aberration andasortof‘system ill- growth on the low average light incomes incum- ness’. The issue was confronted again by Margalef bent upon deep column mixing, especially in et al.(1979), whose ‘mandala’ representation (Fig. high-latitude winters. Limits to the refinement 7.2), based on a reorientation of Margalef’s first of the light-harvesting adaptations required for plot (Fig. 7.1), accommodates a ‘main sequence’ effective operation under such conditions were SPECIES COMPOSITION AND TEMPORAL CHANGE 315

selection, selecting increasingly for the characteristics of R-strategists, and which may well occur in a sequence determined by r–K selectivity. The relevant attributes of the algae favoured by the environmental conditions are shown in Box 5.1 (on p. 212). The corresponding phytoplankton performances and morphologies are also indicated in Figs. 5.8 and 5.10. Smayda and Reynolds (2001)used the same axes to define a ‘habitat template’ (cf. South- wood, 1977)formarine environments. The layout, shown in Fig. 7.4,was conceptual, insofar as the axes are not precisely quantified and merely Figure 7.3 The ‘intaglio’ (of Smayda and Reynolds, 2001), indicative of the ranges of integrated light avail- which allows selection of species within a wide ecological ability and accessible nutrients. The superim- space, according to their primary adaptive life-cycle strategies posed boxes show the approximate positions of (C, R, S), except where nutrients and light are both continuously deficient (the ‘void’). Redrawn with permission specific pelagic habitats and their phytoplankton from Smayda and Reynolds (2001). referred to in the preceding Section (7.2.1). The broad diagonal is included as an approximate border of habitat tenability and separation from recognised, while the combination of low light the voidareas.Italsoservestomaintain the anal- and low nutrients was considered to be unten- ogy with Grime’s (1979, 2001) C–S–R triangular able as suitable habitat for phytoplankton. configuration (Fig. 7.3). There was, by now, a striking resemblance This representation allows us to reflect the between the three viable habitat contingencies observation that the habitats able to support sub- developed from Margalef’s first tentative plot and stantial phytoplankton biomass are those with Grime’s (1979)(seeFig.5.9 and Table 5.3)repre- theleast enduring or least severe constraints sentation of vegetational habitats and the C-, S- of energy and/or nutrient resources. Whereas and R-life-history strategies that plants needed nutrient availability tails off in the downward to adopt to live in them. Reynolds (1988a)pro- direction and harvestable light income dimin- posed the basis of fitting phytoplankton, accord- ishes rightwards, the high-light, high-nutrient ing to their morphologies and physiological sur- habitats in the top left hand corner are chiefly vival adaptations, to the three viable pelagic habi- represented by near-shore habitats and coastal tat combinations of mixing and resource gradi- lagoons, characterised by a potential for high ents (reflecting, respectively, Grime’s ‘duration’ net production and a relatively high support- and ‘productivity’ axes, marked in Fig. 5.9). This ive capacity for planktic biomass. These areas can now be very simply summarised in the form are also relatively rich in the range of species of a diagram (Fig. 7.3). In stable, well-insolated that they are observed to support. The strik- columns, algal uptake is expected to deplete ing association of such waters with outbursts nutrients, making the available resources more of nanoplanktic flagellates, of a variety of phy- inaccessible and demanding specialist adapta- logenetic affinities (prasinophytes, chlorophytes, tions of the phytoplankton for their retrieval. euglenophytes, cryptophytes, chrysophytes and This sets the direction of true autogenic suc- small haptophytes) invokes a common adapta- cession, moving inexorably from r-selected C- tion of small, nanoplanktic size and the poten- strategiststowards K-selected S-strategists. The tially rapid rates of growth conferred by high income of harvestable light and its subjection to unit sv−1 ratios. These properties are shared by the effects on entrainment of the variable mixed the Type-I gymnodinioid and Type-II small peri- depth forms the horizontal axis: mixing events or dinian and prorocentroid dinoflagellates (classi- continuous deep mixing cut across the autogenic fication of Smayda and Reynolds, 2001;Smayda, 316 COMMUNITY ASSEMBLY IN THE PLANKTON

Diminishing I*, increasing hm Figure 7.4 Schematic summary of marine pelagic habitats, along a notional onshore–inshore transect and separating deep-mixed and I well-stratiﬁed systems of varied nutrient deﬁciency. I∗ refers to the T F integral of irradiance received by phytoplankters in mixed-water S T M layers of variable thickness (h ).

O m Redrawn with permission from Smayda and Reynolds (2001).

H P Increasingly inaccessible nutrients

2002)that include Gyrodinium species, Katodinium, tolerance and self-regulation that characterise Heterocapsa triquetra, Scrippsiella trochoidea and Pro- the Group-VII dinophysoids. rocentrum species and which are apparently near- The lower left-hand apex of Fig. 7.5 covers the cosmopolitan among coastal waters. The com- extreme resource-deficient environments of the mon Type-III ceratians (Ceratium fusus, C. furca stratified tropical ocean. The major constraint is and C. tripos)extendintodeepershelfwaters, to gather from the very low concentrations of where they become more abundant in columns essential nutrients, of which phosphorus and, when they are at least weakly stratified, proba- especially, iron may be the most deficient (Karl, bly to within 20–40 m of the surface. Resource 1999). Conforming to the encounter–sufficiency segregation is likely but these larger and more relationship of Wolf-Gladrow and Riebesell (1997) motile dinoflagellates are better adapted to alter- (see also Section 4.2.1), the most efficient pri- nate between satisfying their energy and nutri- mary producers are of picoplanktic size. With ent requirements. These distributions are sepa- abiomass capacity unsupportive of mesoplank- rately shown on the unlabelled template repre- tic phagotrophy, the arguable selective advantage sented in Fig. 7.5. in favour of a dominant SS-strategist picoplank- The shallow mixed, moderately enriched habi- ton (see p. 211)iswell supported by the vast tats of fronts, coastal currents and upwellings are extent and monotony of the Prochlorococcus mono- represented in the centre of Fig. 7.5. These are culture in tropical oceans. Respite comes in able to support smaller nanoflagellates (includ- theform of mixing episodes, stimulating mod- ing a wealth of coccolithophorids at lower lati- est growths of nanoplanktic coccolithophorids tudes) as well as the group of distinctive small, and such specialised microplankters as nitrogen- rounded dinoflagellates that include the harm- fixing Trichodesmium,thediatoms Rhizosolenia styli- ful species Karenia mikimotoi, Lingulodinium poly- formis, R. calcar-avis and Hemiaulus hauckii and edra and Pyrodinium bahamense respectively rep- thedinoflagellates Ornithocercus and Pyrocystis, all resentative of Smayda’s Types IV, V and VI. The of which are incumbent upon hydraulic vari- resource depletion of the upwelling relaxation ations in physical stability. These episodes are zones requires the attributes of low-resource usually relatively short-lived, gradually reverting SPECIES COMPOSITION AND TEMPORAL CHANGE 317

Figure 7.5 Summary of marine pelagic habitats (as shown in Figure 7.4), now populated by functional–morphological categories of phytoplankton (especially of dinoﬂagellates), provisionally identiﬁed by roman numerals: small, rounded gymnodinioids (I) and peridinians (II); migratory ceratians (III); frontal-, upwelling- and current-associated species (IV –VI); heterotrophic dinophysoids (VII), species of the ultraoligotrophic oceans (VIII) and tropical DCM species (IX); for further details, see text. Figure redrawn with permission from Smayda and Reynolds (2001).

to the Prochlorococcus-dominated ambient steady in shallow and inshore areas, including several of state (Karl et al., 2002). thelarge-celled, discoid species of centric diatom, Diatoms are represented almost everywhere such as Cyclotella litoralis, C. caspia and species of within the triangular space in Fig. 7.5.Although Actinocyclus, Cerataulina and Coscinodiscus,that are their basic requirements for light and nutrients encountered also in lower-latitude upwellings. are similar to those of all other phytoplank- Their performances are clearly favoured by rela- ters, satisfaction of two diatom-specific specialist tively high nutrient levels and may depend upon needs – a supply of skeletally progenic silicic acid high levels of insolation. The large group of (SRSi) (see Section 4.7)andfrequent or continu- diatoms whose ranges extend into deeper, but ous entrainment in a surface mixed layer >1–3 still nutrient-rich offshore shelf areas – includ- mindepth(ormoreif only a slow rate of growth ing species of Thalassiosira, Chaetoceros, Leptocylin- can be sustained) (see Section 6.3.2)–isstillpossi- drus, Skeletonema and the slender-celled Rhizosole- ble over all but the extreme left-hand side of the nia species – all show the attenuated antennal template. Nevertheless, a reasonable first suppo- morphologies of R-strategists (sometimes exag- sition is that planktic diatoms of seas and oceans geratedbychain formation). Many of these should invoke the strongly R-strategist adapta- same species appear in the summer plank- tions suited to passive entrainment in highly fluc- tonofthe boreal oceans and polar seas. The tuant, low-average-light environments. restricted diatom flora (Hemiaulus spp., broad- Many of the oceanic and shelf species, indeed, celled Rhizosolenia styliformis and R. calcar-avis)tol- comply with this anticipation. However, the great erant of warm, nutrient-poor but often well- majority of these are found in coastal and near- insolated waters show little tendency towards shore waters, where they are exposed to moder- superior light-harvesting but have special adap- ately high nutrient levels and moderately high tations to contending with chronic nutrient lim- light levels. Some of these are recorded mainly itation Indeed, these diatoms show characters of 318 COMMUNITY ASSEMBLY IN THE PLANKTON

more K-selected S-strategists and they may be per- structures of distinct pelagic ecosystems. Platt haps considered as intermediate RS-strategists. and Sathyendranath (1999)visualised globally Several other general deductions about the segregated provinces of the sea, distinguished by composition of planktic communities generally their susceptibility to environmental forcing, the and the functional role that they fulfil emerge primary production that each might sustain and from the patterns identified. One relates to the thefates of their primary products. The species of high species richness of the relatively benign phytoplankton at the hearts of these structures environments that are not hostile to the majority are, often, both the architects of the processing of species as a consequence of severe resource and and the best-fitted respondents to the prevailing energy constraints. Extremes in either direction environmental constraints. lead to the failure of all those species that lack the adaptations to be able to tolerate the increas- 7.2.3 Species assemblage patterns in lakes ingly exacting circumstances – species richness To review the composition of phytoplankton in a is ‘squeezed out’ (Reynolds, 1993b). The toler- diverse range of inland waters – great lakes and ant survivors are, by definition, well-adapted spe- small lakes, deep and shallow, saline and soft, cialists and their presence in low-diversity com- acidic and calcareous, rivers, reservoirs, ponds – munities constitutes a robust indicator of the in anything like the same way as was done for the particular severe conditions. More, their pres- sea (Section 7.2.1)would be a daunting exercise, ence will always help to identify the function for author and reader alike. Fortunately, there of species clusters associated with slightly less is an easier course to be steered, although the extreme circumstances (Dufrêne and Legendre, rules ofnavigation need some prior explanation. 1997). Because less exacting conditions are acces- Part of a personal quest to be able to define what sible to many more species, more outcomes are algae live where and why (Reynolds, 1984a) has, possible and, thus, they tend to lack positive over a period of 20 years, developed a tentative species identifiers. and still-evolving phytoplankton flora (Reynolds Secondly, species-poor, highly selected assem- et al., 2002). Cataloguing natural assemblages of blages of species will dominate the behaviour of phytoplankton species generally reveals interest- the community and control the fate of primary ing patterns. Not only are many species observed products. For instance, assemblages dominated periodically in a given lake but their periodicity is by diatoms are most liable to the dynamic con- also generally quite regular. Moreover, they often trols set by sinking loss rates. Biomass is mainly co-occur with other species whose numbers fluc- exported to depth, where it is processed by ben- tuate similarly and broadly simultaneously, as if thic or bathypelagic consumers through spatially in response to the same seasonal or environmen- large recycle mechanisms. Heavy grazing may tal drivers. Further, in part or in whole, the same reduce the direct sedimentation of phytoplank- clusters of co-occurring species are recognised in ters but, in part, substitute a flux of zooplankton other water bodies, despite mutual hydrological cadavers, faecal pellets and an export of particu- isolation in many instances, and in what appear late silica. Planktic primary products are more to similar kinds of water bodies but at remote dis- likely to be accumulated in the pelagic if the tances. In between times and at many other loca- algae are simultaneously small and ungrazed. tions, these species clusters are not represented. Export is proportionately least when most of the They may well be replaced in abundance by quite carbon is fixed by picophytoplankton and pro- different sets of co-occurring species but which, cessed through a microbial food web (Legendre nevertheless, form equally distinctive, recurrent and LeFevre, 1989). clusters. Finally, it is the matching of processes to func- The pattern is scarcely obscure but it is diffi- tional groups of phytoplankton species and, in cult either to describe or to explain. Before the turn, to the overriding environmental circum- days of the sophisticated and readily available stances biassing their selection, that leads to the statistical packages, the best-known techniques elaboration and definition of macroscale spatial were those introduced by the European school of SPECIES COMPOSITION AND TEMPORAL CHANGE 319 phytosociologists to diagnose plant communities et al., 2003;Naselli-Flores and Barone, 2003; and associations (Tuxen,¨ 1955;Braun-Blanquet, Naselli-Flores et al., 2003). The scheme is still 1964). They would make a list of species in each evolving and two further algal groups have since of a series of intuitively judged small areas of been proposed (Padisak´ et al., 2003c). A new con- uniform vegetation, called relevés, scoring for the fusion is the fact that some species are correctly relative area covered by each species. Listing the classifiable in more than one cluster, according species in the same order made it easy to build up to their life histories (see p. 269). frequency tables in which regularly co-occurring However, the scheme is not just about recog- species are blocked together, while those that nising and giving labels to groups. The species are avoided will appear in other blocks. These forming the particular groups have demonstra- blocks, or associations, can be named and classi- bly similar morphologies, environmental sensi- fied, just as if they were individual species. The tivities and tolerances, and they are not necessar- task of explaining the ecologies of the compo- ily confined to one phylogenetic group (Reynolds, nent species is arguably easier to progress if the 1984b, 1988a). They feature prominently the vagaries of variable presence or relative impor- strategic adaptations that are required in the tance of individual species is suborned to the habitats in which they are known to be capable higher level of the species cluster. of good growth performances (Reynolds, 1987b, Confronting accumulating records of species 1995a). These various aspects were summarised counts in preserved samples collected weekly in tabular form in Reynolds et al.(2002). The (sometimes more frequently) from each of several coda can be used to represent seasonal changes in separate water bodies, I applied myself to the very dominance (Naselli-Flores et al., 2003), responses tedious task of treating each count as a phyto- to eutrophication (Huszar et al., 2003)andthe sociological relevé and to diagnosing species that effects of non-seasonal physical forcing (Reynolds, co-occurred frequently, rarely or not at all. Some 1993b). weighting for larger species occurring in small The groupings themselves are tabulated in numbers was the only modification needed to Table 7.1 forreference. Their properties are briefly diagnose 14 such species-clusters that were ade- noted but these are also amplified in the context quate to describe the entire seasonal periodic- of the compositional patterns observable in the ity of the phytoplankton in five contrasted lakes freshwater systems exemplified. in north-west England and five managed annual sequences in the Blelham experimental enclo- Phytoplankton of large oligotrophic and sures (Fig. 5.11). The clusters were not identified ultraoligotrophic lakes beyond an alphanumeric label but the patterns We start with examples of the phytoplankton and periodic sequences were conveniently ratio- assemblages that are encountered in some of nalised in these terms (Reynolds, 1980a). theworld’s larger lakes. According to Herden- The original scheme has been much modified, dorf (1982), 19 of the inland waters currently mainly through the addition of more alphanu- on planet Earth have areas greater than 10 000 meric groups to embrace algal assemblages in km2 and another 230 are greater than 500 km2. other types of water and in many other global Together, they contain about 90% of its inland locations. Most of the new groupings have been surface water. To put these in a single cate- delimited using statistical methods, which, inci- gory of ‘large lakes’ can be justified only in the dentally, have been used to validate almost all present context of waters overwhelmingly domi- the originalones.Someofthese have been sub- nated by open-water, pelagic habitats. Here, the divided or realigned slightly in arriving at the grouping will exclude examples that are ‘shal- 31 groups defined byReynoldset al.(2002). Sev- low’. This term itself requires careful definition; eral independent studies have been able to apply following Padisak´ and Reynolds (2003), shallow- and amplify the scheme without undue contro- ness is only sometimes a self-evident absolute. versy and, thus, help to confirm its utility (Kruk The statement that a lake is ‘relatively shal- et al., 2002; Dokulil and Teubner, 2003;Leitão low’ is based upon the ratio between absolute 320 COMMUNITY ASSEMBLY IN THE PLANKTON

Ta b l e 7.1 Trait-separated functional groups of phytoplankton

Group Habitat Typical representatives Tolerances Sensitivities A Clear, often well-mixed, Urosolenia, Cyclotella Nutrient deficiency pH rise base-poor lakes comensis B Ver tically mixed, Aulacoseira subarctica, A. Light deficiency pH rise, Si mesotrophic islandica depletion, small–medium lakes stratification C Mixed, eutrophic Asterionella formosa Light, C Si exhaustion, small–medium lakes Aulacoseira ambigua, deficiencies stratification Stephanodiscus rotula D Shallow, enriched turbid Synedra acus, Nitzschia Flushing Nutrient depletion waters, including spp., Stephanodiscus rivers hantzschii N Mesotrophic epilimnia Tabellaria, Cosmarium, Nutrient deficiency Stratification, pH Staurodesmus rise P Eutrophic epilimnia Fragilaria crotonensis, Mild light and C Stratification Si Aulacoseira granulata, deficiency depletion Closterium aciculare, Staurastrum pingue T Deep, well-mixed Geminella, Mougeotia, Light deficiency Nutrient deficiency epilimnia Tribonema S1 Turbid mixed layers Planktothrix agardhii, Highly Flushing Limnothrix redekei, light-deficient Pseudanabaena conditions S2 Shallow, turbid mixed Spirulina, Arthrospira Light-deficient Flushing layers conditions SN Warm mixed layers Cylindrospermopsis, Light-, nitrogen- Flushing Anabaena minutissima deficient conditions Z Deep, clear, mixed layers Synechococcus, Low nutrient Light deficiency, prokaryote grazing picoplankton X3 Shallow, clear, mixed Koliella, Chrysococcus, Low base status Mixing, grazing layers eukaryote picoplankton X2 Shallow, clear mixed Plagioselmis, Stratification Mixing, layers in Chrysochromulina filter-feeding meso-eutrophic lakes X1 Shallow mixed layers in Chlorella, Ankyra, Stratification Nutrient deficiency, enriched conditions Monoraphidium filter-feeding Y Usually small, enriched Cryptomonas, Peridinium Low light Phagotrophs! lakes lomnickii E Usually small, Dinobryon, Mallomonas Low nutrients CO2 deficiency oligotrophic, (Synura) (resort to base-poor lakes or mixotrophy) heterotrophic ponds (cont.) SPECIES COMPOSITION AND TEMPORAL CHANGE 321

Ta b l e 7.1 (cont.)

Group Habitat Typical representatives Tolerances Sensitivities

F Clear epilimnia Colonial chlorophytes Low nutrients ?CO2 deficiency, like Botryococcus, high turbidity Pseudosphaerocystis, Coenochloris, Oocystis lacustris G Short, nutrient-rich Eudorina, Volvox High light Nutrient deficiency water columns J Shallow, enriched lakes Pediastrum, Coelastrum, Settling into low ponds and rivers Scenedesmus, light Golenkinia K Short, nutrient columns Aphanothece, Deep mixing Aphanocapsa H1 Dinitrogen-fixing Anabaena flos-aquae, Low nitrogen, low Mixing, poor light, nostocaleans Aphanizomenon carbon low phosphorus H2 Dinitrogen-fixing Anabaena lemmermanni, Low nitrogen Mixing, poor light nostocaleans of larger Gloeotrichia echinulata mesotrophic lakes U Summer epilimnia Uroglena Low nutrients CO2 deficiency LO Summer epilimnia in Peridinium willei, Segregated Prolonged or deep mesotrophic lakes Woronichinia nutrients mixing LM Summer epilimnia in Ceratium, Microcystis Ver y lowC, Mixing, poor light eutrophic lakes stratification M Dielly mixed layers of Microcystis, High insolation Flushing, low total small eutrophic, low Sphaerocavum light latitude R Metalimnia of Planktothrix rubescens, Low light, strong Instability mesotrophic stratified P. mougeotii segregation lakes V Metalimnia of eutrophic Chromatium, Chlorobium Very low light, Instability stratified lakes strong segregation W1 Small organic ponds Euglenoids, Synura, High BOD Grazing Gonium W2 Shallow mesotrophic Bottom-dwelling ?? lakes Trachelomonas (e.g. T. volvocina) Q Small humic lakes Gonyostomum High colour ?

Source: Updated from Reynolds et al.(2002). depth and wind fetch and the ability of a lake physical recycling and the frequency access of to maintain a density-differentiated stratiﬁca- phytoplankton to resources accumulated by and tion for some weeks or months on end (see discharged from the deeper sediments. For many Fig. 2.19). The relevance of the distinction is years, the bathymetry of (and, hence, the vol- the extent to which the plankton-bearing sur- ume of water stored in) large lakes remained less face waters are affected by the internal rates of familiar than their respective areas. Several have 322 COMMUNITY ASSEMBLY IN THE PLANKTON

been added to the category of ‘deep lakes’, even confined to the stratified periods (Kozhov, 1963; since Herdendorf’s (1990)listing. These include Kozhova, 1987;Kozhova and Izmest’eva, 1998; Lago General Carrera/Buenos Aires, straddling Goldman and Jassby, 2001;Popovskaya, 2001). the Chile/Argentina border, Danau Matano in The spring development, which takes place under Indonesia and Lake Vostok, Antarctica. ice, is subject to sharp interannual variability. In Setting aside those that are saline (relatively) high-production years, diatoms (espe- (Kaspiyskoye More, Aralskoye More), the natural cially Aulacoseira baicalensis, A. islandica, Nitzschia condition of the water in most of these large, acicularis, Synedra ulna var. danica and Stephano- deep lakes is to be deficient in nutrient resources. discus binderanus), small dinoflagellates (includ- They occupy large basins, fashioned either by ing Gymnodinium baicalense) and chrysophytes tectonics or scraped out by glacial action, and (especially Dinobryon cylindricum)are prominent are presently filled with water that is renewed (Popovskaya, 2001). Although several of these only very slowly. Large lake volumes in relation algae are endemic, the assemblage corresponds to catchment area also make for low support- mainly to Association-B diatoms, which have ive capacities and, indeed, the phytoplankton ahighsv−1,and whose growth is tolerant of they carry is typically dilute. Where known low temperature, poor insolation and low phos- (or where approximated from published bio- phorus concentrations (Richardson et al., 2000), volume estimates), average seasonal maxima with some representatives of the E-andY-groups of chlorophyll are <4mgchla m−3,although of flagellates. In low-production years, all algae greater concentrations may be found locally are scarce (the interannual difference in pop- (Reynolds et al., 2000). In many instances, the ulations of dominant Aulacoseira baicalensis is paucity of phytoplankton may be determined between 100–200 cells mL−1 to1to2ordersof principally by energy limitation in deep, mixed magnitude fewer: (Popovskaya, 2001). The critical layers. variable seems to be the extent of snow cover Among the most systematically studied of on the ice: besides letting more light through, these large lakesisOzeroBaykal.Formedinagap snow-free ice allows more rapid heating of water between two separating tectonic plates, Baykal is directly beneath the ice, which then sinks to the also the deepest (1741 m), stores the greatest vol- point of isopycny, some 10–20 m below. This sets ume (nearly 23 000 km3)andisprobably the old- up a convective motion which resembles the epil- est (∼20 Ma) of all the world’s lakes. Despite sig- imnion of a warm, ice-free lake (Rossolimo, 1957). nificant industrialisation and settlement of the Indeed, this structure allows rather better inso- catchment (especially around Irkutsk) and pol- lation of entrained diatoms than is possible in lution of its two major inflows (Angara, Selenga theice-free column, until surface heating allows Rivers), the lake remains oligotrophic in charac- the lake to stratify directly (maximum surface ter. Retention time is estimated to be 390 a. In temperatures may then reach 12–16 ◦C: Nakano the offshore areas, levels of soluble phosphorus et al., 2003). Then, algae tolerant of stratifica- (SRP) and dissolved inorganic species of nitrogen tion, high insolation and low nitrogen and phos- (DIN) are <15 µgPand<100 µgNl−1 (Kolpakova phorus concentrations (F-group colonial chloro- et al., 1988;Goldman and Jassby (2001). The lake is phytes, including Botryococcus, and potentially classically dimictic. Near-surface warming of the nitrogen-fixing Anabaeana lemmermannii of group watersurface in the summer induces thermal H2:Goldman and Jassby, 2001;Popovskaya, 2001) stratification (July to September); in the winter, predominate. However, the main pelagic primary the lake isice-covered from January to late May. producers in summer are group-Z picoplanktic At other times, the lake is subject to deep con- Cyanobacteria: in Baykal, populations of Syne- vective mixing that is sufficiently intense to aer- chocystis limnetica may exceed 105 cells mL−1,are ate the profundal waters (Rossolimo, 1957;Vot- responsible for, perhaps, 80% of the pelagic pri- intsev, 1992). Despite substantial year-to-year vari- mary production and support a well-developed ations in the production and standing biomass microplanktic food web (Nakano et al., 2003). Like of phytoplankton, it is plain from each of the Prochlorococcus in the tropical sea, they are able to main overviews that increase of both is mainly function in clear, well-insolated water, turning SPECIES COMPOSITION AND TEMPORAL CHANGE 323 over fixed carbon to the microbial heterotrophs, of the surface), phytoplankton increases during whilst nevertheless maintaining a weakly grazed spring to a maximum of ∼7 µgchla L−1 in biomass. June. A second peak in August has about half Lake Superior covers a larger area than Ozero this magnitude (Munawar and Munawar, 2001). Baykal (82 100 against 31 500 km2)butitsdepth In Lake Michigan (area 57 750 km2,mean depth (maximum 407 m, mean 149 m) and volume 85 m, TP 5–8.5 µgPL−1,DIN≤260 µgNL−1, (12 200 km3)areinferior(Herdendorf, 1982). Its stratified July–September to within 20–30 m of basin is tectonic in origin but was significantly thesurface), a similar diacmic pattern of abun- scoured by ice during the last (and possibly pre- dance is observed, with maxima in June and vious) glaciation. The present lake is little more August. The earlier is larger (maximum ∼11 than 15 ka in age (Gray et al., 1994). The lake area µgchla L−1)thanthesecond. The dominant is large relative to that of the drainage basin; species are similar in either case: diatoms of currently, the hydraulic retention time is around the A-group (Cyclotella spp., notably C. bodan- 170 a.Theinputofnutrients has for long been ica, C. radiosa, C. glomerata;alsoUrosolenia erien- very low and, except in the vicinity of industri- sis)andsuch B-group representatives as Aulaco- alised cities like Duluth and Thunder Bay, con- seira islandica and Tabellaria flocculosa are rela- centrations of TP (3.5–7.0 µgPL−1), SRP (≤3 µgP tively abundant throughout and dominate the L−1)andDIN(≤300 µgNL−1)are typically dilute. earlier peak. Nanoplanktic flagellates of the X2 Annual TP loads are <0.1gm−2 a−1 (Vollen- group (Chrysochomulina, Ochromonas)andE- and U- weider et al., 1974). The phytoplankton biomass groups of microplanktic chrysophytes (Dinobryon (supposed to average ∼1–1.5 µgchla L−1)iscor- spp., Mallomonas spp., Uroglena spp.) are relatively respondingly modest and the water (Secchi-disk more abundant during the second peak, when transparency 10–17 m: Gray et al., 1994). How- picoplanktic Chroococcoids (Z)arealsoat their ever, for much of the time, low water temper- most numerous (Munawar and Munawar, 2001). atures and weak insolation may provide more Comparison with the findings of Johnson (1975, severe production constraints. Enhanced produc- 1994)showsthat similar species assemblages tion and elevated phytoplankton biomass in the make up the very sparse ‘peaks’ (probably <0.5 µg open water are noted between July and October, chla L−1)ofphytoplankton biomass encountered when surface water temperatures are sufficiently at the beginning and towards the end of the ice- differentiated for mixing to be restricted to the free period (July–November) in Great Bear Lake upper 20–30 m, allowing weak summer stratifica- (area 31 150 km2, mean depth 72 m, SRP ≤0.1 µg tion (Munawar and Munawar, 1986, 2000, 2001). PL−1). According to these synopses, diatoms (especially Since the late 1980s, the Laurentian Great Cyclotella radiosa and Tabellaria fenestrata)develop Lakes have been experiencing the spread of a at the start of this period, followed by nanoplank- Eurasian alien, the bivalve Dreissena polymorpha. tic phytoflagellates of the genera Cryptomonas, Its motile larvae have taken great advantage of Plagioselmis, Ochromonas and Chrysochromulina and the canal systems of Europe and the ballast tanks microplanktic Uroglena.Picoplanktic chroococ- of ocean-going ships to spread from its native coid Cyanobacteria become numerous (Munawar areas of the Caucasus to the Atlantic seaboard and Fahnenstiel, 1982;Fahnenstiel et al., 1986) (by the mid twentieth century) and, eventually, and, despite being a small part of the phyto- to theStLawrence basin. The mollusc colonises plankton biomass, contribute significantly to the almost any firm submerged surface where, multi- annual carbon budget (∼50 C m−2 a−1). The plied by its numbers and explosive reproductive sequence of phytoplankton can be summarised performances, its dense aggregations can gener- A/B → X2/Y → U → Z. ate significant filtration capacities. Dreissena has Superior’s neighbouring Great Lakes are sim- been particularly successful in Lake Erie and the ilar in the modesty of phytoplankton they sup- Saginaw Bay area of Lake Huron where its inva- port. In Lake Huron (area 59 500 km2,meandepth sion has contributed to the reduction in phyto- 59 m, TP 5–7 µgPL−1,DIN≤300 µgNL−1, plankton and TP content of the water (arguably stratified July–September to within 20–30 m more so than newly imposed statutory pollution 324 COMMUNITY ASSEMBLY IN THE PLANKTON

controls) and improvements in clarity and macro- (Reynolds et al., 2002). Lake Ontario supports an phyte growth (Nalepa and Fahnenstiel, 1995). abundant chroococcoid picoplankton in summer Among the other large North American lakes, and whose dynamics and distribution were the thespring phytoplankton generally includes subject of a detailed study by Caron et al.(1985). awider range of diatoms. Various studies Diatoms occur throughout the year in Lake (Munawar and Munawar, 1981, 1986, 1996; Ontario but, during the early part of the year, Duthie and Hart, 1987;Pollingher, 1990)reveal Stephanodiscus binderanus,especially, ‘blooms’ in that C-group Asterionella formosa and Stephan- thenear-shore areas of the lake, where popu- odiscus binderanus are well represented in the lations become substantially isolated by a phe- plankton of Great Slave Lake (area 27 200 km2, nomenon known as ‘thermal barring’. This was mean depth 58 m, TP: 3–8 µgPL−1,ice-free described in detail by Munawar and Munawar June–November, stratified to within ∼30mofthe (1975)but it is now known to be a common surface July/August: details from Moore, 1980), feature in other large, cold-water lakes, includ- Lake Erie (area 25 660 km2 mean depth 19 m, ing Michigan (Stoermer, 1968), Ladozhskoye and TP 11–45 µgPL−1)andLake Ontario (area 19 100 Onezhskoye (Raspopov, 1985;Petrova,1986)and km2 mean depth 86 m, TP 10–25 µgPL−1,like Baykal (Shimarev et al., 1993; Likhoshway et al., Lake Erie, it is stratified to within ∼22 m of the 1996). In essence, vernal heating proceeds more surface June–October). In the eastern and cen- rapidly in the shallow near-shore waters than in tral basins of Lake Erie, phytoplankton biomass theopen, offshore areas of the lake but, while develops during June culminating in summer temperatures remain <4 ◦C, the warmer water (August) maxima in the order of up to 30 µgchla is retained within inshore circulations separated L−1 and in which small dinoflagellates (especially from the open lake by pronounced frontal bound- Gymnodinium helveticum, G. uberrimum and Glen- aries. The slightly higher temperatures and the odinium spp.) and Cryptomonas species are com- rather higher average insolation experienced by mon reprsentatives of a Y-type assemblage. There thealgae thus retained promotes the early-season is also a well-developed nanoplankton in which growth and recruitment of phytoplankton, domi- X2-group Plagioselmis and Chrysochromulina are nated by group-C diatoms, group-Y flagellates and joined by Chlorella, Monoraphidium and Tetraedron nanoplankton. species, all X1-group, overtly C-strategist species The phytoplankton of the two northern great whose growth requires higher half-saturation lakes of Eurasia shows closer affinites to that concentrations of SRP (Section 5.4.4). Chroococ- of Baykal, Erie and Ontario than to that of the coid picoplankters (Z)arealsopresent in the sum- upper Laurentian Great Lakes. In Ladozhskoye mer. In the shallower and most enriched western Ozero (area 18 140 km2, mean depth 50 m, TP: basin of Lake Erie, there is a substantial spring 13–40 µgPL−1,ice-covered February–May, strat- bloom dominated by Stephanodiscus binderanus ified July–August, but very variable stability), a and other B-andC-group diatoms, abundant flag- spring diatom bloom of B-andC-group diatoms ellates of group Y and Pediastrum and Scenedesmus, (including Aulacoseira subarctica, A. islandica, Asteri- representing the J group of eutrophic chloro- onella formosa, Diatoma spp.), apparently nur- coccaleans. The offshore phytoplankton of Lake tured in thermal-bar conditions (see above and Ontario behaves similarly to that of eastern p. 89), spreads through the lake (chla gener- Lake Erie, except that the summer plankton is ally 1–5 µgL−1). Asterionella continues to domi- more biassed towards dominance by mucilage- nate the unstable open lake conditions, together bound, non-motile, colonial chlorococcalean and with variable quantities of group-P Aulacoseira tetrasporalean genera of green algae (group F) granulata and Fragilaria crotonensis.Often,signif- such as Oocystis, Coenochloris and Pseudosphaerocys- icant quantities of filamentous Cyanobacteria tis.Hutchinson (1967) called these ‘Oligotrophic (especially Planktothrix agardhii of group S1)and chlorococcal plankters’; it is a widespread group xanthophytes (Tribonema of group T)are selected (see below) that survives low SRP concentrations by their tolerance of low average insolation but is apparently intolerant of poor insolation in mixed conditions (Raspopov, 1985). Under SPECIES COMPOSITION AND TEMPORAL CHANGE 325 calmer conditions, the Cyanobacteria Aphan- Phytoplankton of smaller temperate izomenon and Woronichinia sometimes form sig- oligotrophic lakes nificant blooms. I have no information to hand The ‘small-lake’ category as adopted here applies concerning the nano- and picoplankton but to waters <10 km2. Whilst most of the fresh water the dominant calanoid zooplankton and well- is stored in ‘large’ lakes (>500 km2), most of the developed ciliate microplankton are suggestive world’s lakes (∼8.4 × 106 in total: Meybeck, 1995) of an active microbial food web. In Onezh- are ‘small’. A further 13 450 in the range 10–500 skoye Ozero (area 9 900 km2,meandepth 28 m, km2 might be described as ‘medium-sized’. So TP 5–10 µgPL−1,ice-covered January–May, far asisknown,alargeproportionofthese thereafter, thermal bar formation separates the represents lakes in unyielding rocky basins and inshore from the isothermal circulation of the forested catchments and the phytoplankton car- central water mass; stratification develops from rying capacity is unambiguously constrained by July to September, to within 30 m from the sur- the availability of nutrient resources, rather than face), the spring assemblage is dominated by B- by low temperatures and low insolation. Their group Aulacoseira and C-group Asterionella. The sea- smaller sizes facilitate a high frequency of sam- sonal progression passes by way of Tabellaria to ple collection and a robust picture of seasonal asequence of oligotrophic–mesotrophic assem- change in production and biomass as well as blages featuring Dinobryon (E)species, Coenochlo- species composition. In previous work (Reynolds, ris (F)species, Woronichinia (LO)andPlanktothrix 1984a), I have cited Findenegg’s (1943)thorough agardhii (S1)but the biomass at the summer max- two-year (1935–36) survey of the phytoplankton imum scarcely exceeds 6 µgchla L−1 (Kauffman, in some 15 moderately alkaline lakes of Karnten¨ 1990). (Carinthia), Austria, to exemplify the genre (in In Ozero Issyk-kul (area 6 240 km2,mean particular, Millstatter¨ See: area 13.3 km2,mean depth 279 m, TP 2–4 µgPL−1,stratified depth 86.5 m, stratified May–November to within April–December, to within ≥13mofthesurface: 7–10 m of the surface, TP, not reported but SRP Shaboonin, 1982), relative phytoplankton abun- <1 µgPL−1,DIN≤300 µgNL−1). There is a sin- dance is diacmic. The earlier (May) peak involves gle(monacmic) summer biomass ‘maximum’ in group-A Cyclotella species and group-B Aulacoseira summer (chla ∼1.5 µgPL−1 (Fig 7.6), when the species the later (October) peak is dominated A-group spring diatoms (Cyclotella comensis, C. glom- by the Cyanobacterium Merismopedia and the erata)aresupportedbyamixture of other species dinoflagellate Peridinium willei which both rep- that include self-regulating dinoflagelleates (Peri- resent group LO.Species of Coenochloris, Oocys- dinium willei,some Ceratium hirundinella)and tis, Gloeocapsa, Lyngbya,aswellasan‘abundant colonial Cyanobacteria, now known as Woroni- nanoplankton’ also feature in this faintly saline chinia (representing group LO), and such (N-group, lake (Savvaitova and Petr, 1992). high-nutrient-affinity) desmids as Staurodesmus In conclusion, the phytoplankton of large, species Findenegg (1943)alsorecorded species high-latitude lakes involves elements character- of Coenochloris, Oocystis, Gymnodinium, Rhodomonas ising either some of the ultraoligotrophic func- and other nanoplankters, as well as the non-gas- tional groups, distinguished by their high affin- vacuolate, unicellular Cyanobacteria Chroococcus ity for phosphorus (A, Z), or other substantially and Dactylococcopsis. Moreover, Findenegg (1943) oligotrophic groups (B, X2, E, F, LO, U)toler- found similar assemblages in several of the other ant of low nutrient concentrations (especially of lakes intheregion: inWorthersee,¨ Uroglena and, phosphorus). However, there is no clear evidence especially, Planktothrix rubescens, constituted met- that these algae habitually fill the nutrient- alimnetic maxima. Findenegg’s explanation for determined capacity, except when average inso- theseasonally distinctive assemblages and dis- lation allows it. Excess of nutrient capacity over tributions invoked the interaction of light and average light income favours the R-strategies of temperature preferences of participating algae. the C, P, S and T groups of attenuated and fila- The four contingencies (cold-water, low-light mentous ‘antennal’ algae. forms; cold-water, high-light forms; warm-water, 326 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.6 Annual cycles of phytoplankton biomass (as measured or approximated from biovolume) in some temperate lakes: (a) Millst¨attersee, 1935 (after Findenegg, 1943); (b) Windermere, North Basin, 1978 (Reynolds, 1984a); (c) Sj¨on Erken, 1957 (Nauwerck, 1963); (d) Crose Mere, 1973 (Reynolds, 1976a). Redrawn from Reynolds (1984a).

high-light forms; warm-water, low-light forms) (F-group Coenochloris, Oocystis), then desmids approximated to winter, spring, summer and (Staurastrum spp.), before Aulacoseira ambigua and autumn plankton. other spring diatoms are entrained from the Other small, low-nutrient lakes show simi- deepest layers. lar seasonality, involving similar species of alga. In Finland, many small lakes are simul- Hino et al.(1998)recentlypublished the results taneously soft-watered, oligotrophic and often of an investigation of a small, low-alkalinity lake strongly humic. The high latitude and short win- in Hokkaido, Japan (Akan-Panke: area 2.8 km2, ter days greatly constrain the ability of phyto- mean depth 24 m, TP ≤10 µgPL−1,DIN≤300 plankton to sustain net photosynthetic gain. µgNL−1,stratified May–October to within 5 Any growth at these times must be sustained mofthesurface,ice-covered November–May). heterotrophically; few surviving cells even con- This lake is classically dimictic but the overturn tain chlorophyll (Arvola and Kankaala, 1989). periods are brief; the lake is usually stratified However, there are some species of Chlamy- and its resources become strongly segregated. domonas, Chlorogonium, Peridinium and Gymno- −1 The water has a high clarity (εmin ∼0.15 m , dinium that are able to maintain high population Secchi-disk transparency 7–18 m). The spring densities just below the surface while ice cover overturn (maximum, 2–3 µgchla L−1)isdom- persists (Arvola and Kankaala, 1989). inated by diatoms (A-, B-andC-group species In Stechlinsee, another well-studied olig- include Cyclotella radiosa, Asterionella formosa and otrophic system (area: 4.3 km2, mean depth 22.8 Aulacoseira ambigua). As they settle out (taking m, TP ≤16 µgPL−1, DIN ≤95 µgNL−1,stratified most of the bioavailable P and TP with them, May–October, to within 7–10 m of the surface, the epilimnion is left with a sparse population ice-covered January–March: details from Gervais of E-group chrysophytes (particularly Dinobryon et al., 1997), the phytoplankton biomass peaks in cylindrica). By summer, the surface waters are spring, dominated by A-group Cyclotella species substantially depleted of all but chroococcoid and picoplanktic Cyanobacteria (Padisak´ et al., picoplankters and chlorococcal nanoplankters 1998). Development starts in February or March (together accounting for <1 µgchla L−1). Dom- and is terminated by the onset of the summer inant microplankters (in which U-group Uroglena stratification and the sinking of the diatoms into americana and LO-group Peridinium aciculiferum thehypolimnion. Exhaustion of the epilimnetic and Merismopedia are prominent) are based in nutrient base confines autotrophic production themetalimnetic region (at a depth of 10–25 m). to the metalimnion but, in this lake, it is the With increasing mixed depth towards the end picoplanktic Cyanobacteria that dominate both of the summer, there are first more green algae thebiomass and the production (see also Gervais SPECIES COMPOSITION AND TEMPORAL CHANGE 327 et al., 1997). Originally identified as a Synechococcus zooplankton abundance but both seemed to be species. the alga is now recognised as Cyanobium incidental to the continuing predominance of (Padisak,´ 2003). Peridinium. The success of the alga relates to its In the 20 years covered by the study of Berman efficient perennation and its ability to exploit its et al.(1992), the phytoplankton periodicity of mobility to ‘scavenge’ (or ‘glean’) the water col- Yam Kinneret (Sea of Galilee) showed great inter- umn of its nutrient reserves during the early stag- annual similarity in the abundance, distribu- nation period. Depletion of both phosphorus and tion and composition of the phytoplankton. This nitrogen to the limits of detection attests to the warm monomictic rift-valley lake in the upper efficiency of this process. The post-bloom phyto- Jordan Valley (area 168 km2,mean depth 25.5 plankton is redolent of other very oligotrophic m, stratified March–December) experiences a typ- pelagic systems where the primary products of ically Mediterranean climate, with rainfall con- similar organisms are tightly coupled within fined to the winter period (Serruya, 1978). It is microbial food loops. Such interannual variations briefly isothermal with a minimum temperature in the size of the Peridinium crop as had been of ∼13 ◦Cbut, by April, is generally strongly strat- observed seem to be inverse to the fluctuations in ified to within 10 m of the surface, as epilim- Aulacoseira production: years with larger diatom netic temperatures reach 30 ◦C. Its waters are maxima heralded smaller Peridinium maxima. mildly alkaline and slightly saline. The maxi- Interestingly, variations to the stable sequence mum bioavailability of both nitrogen and phos- have been observed in the 1990s. There have been phorus is modest (≤200 µgNL−1, ≤5 µgPL−1). one or two years when the excystment and spring In each of the years from 1970 to 1989 inclusive, recruitment of Peridinium has been poor and the phytoplankton developed in a characteristic green algae or Microcystis becoming briefly abun- way. Starting with the autumnal circulation, the dant. The summer appearance of nitrogen-fixing main components were unicellular Cyanobacte- Anabaena ovalisporum,in1994andinoneortwo ria (Chroococcus)andsuch (X2-) nanoflagellates as subsequent years, is another departure from the Plagioselmis and Chrysochromulina.Withfullover- stable pattern. The tempting explanation is that turn and winter flooding, coenobial and filamen- the increase in phosphorus loading has triggered tous plankton develop, including the apparently these events but careful analysis shows a trend of warm stenothermic diatom, Aulacoseira granulata, decreasing winter concentrations in the lake and of Group P.Atthis time, there would also be alengthening of the period of thermal stratifica- excystment of the large, self-regulating dinoflag- tion (Hambright et al., 1994). Berman and Shtein- ellate now known as Peridinium gatunense and man (1998) also comment on the effect of a weak- ascribed by Reynolds et al.(2002)toGroup LM. ening of diffusivity in the water column working Under conditions of reduced vertical mixing, this against the selective exclusivity in favour of Peri- alga typically built to a stable maximum, often dinium at critical points in its annual cycle. lasting from March to May, which represented The last example in this section is from Biwa- the greatestannual biomass. Its termination, ko, which, on criteria set in this chapter, is through encystment and settlement, generally really a ‘large lake’ (area 674 km2,mean depth coincided with high epilimnetic temperatures 41 m, TP ≤10 µgPL−1,DIN≤350 µgNL−1, (between 27 and 30 ◦C) and virtual exhaustion of stratified April–November to within 20 m of the the epilimnetic reserve of nitrogen. The summer surface: Nakamura and Chang, 2001). Its phyto- biomass remained relatively very low, comprising plankton was described in detail by Nakanishi asparsenanoplanktonand numerous picoplank- (1984) but ongoing concerns about the water ton (Malinsky-Rushansky et al., 1995). Metalim- quality and the appearance of Microcystis pop- netic layers tended to be dominated more by ulations in the lake (which supplies drinking group-V photobacteria (Chlorobium)than algae. waterto15Mpeople in Kyoto and Osaka) have Berman et al.(1992)wereconcerned to inter- encouraged frequent monitoring of the plank- pret this interannual stability against a trend ton. The winter plankton of the mixed water of rising phosphorus loads and to fluctuating column is sparse and dominated by Aulacoseira 328 COMMUNITY ASSEMBLY IN THE PLANKTON

solida (Group B?) with increasing quantities of (Vicente and Miracle, 1988;Guerrero and Mas- Asterionella formosa (group C)through spring and Castellà, 1995)andPlanktothrix of the rubescens asummerassemblage of Staurastrum dorsiden- group (R)(Findenegg, 1943;Zimmermann, 1969; tiferum, Closterium aciculare and Aulacoseira gran- Bright and Walsby, 2000). Cryptomonas species ulata (group P). Since 1977, Uroglena americana (group Y)alsomaintain stable layers in karstic has ‘bloomed’ each spring (maximum 6–10 µg dolines (Pedros-Ali´ o´ et al., 1987;Vicente and Mir- chla L−1)and, since 1983, small numbers of acle, 1988)and,attimes,inlarger lakes (Ichimura (group H) Anabaena and (group LM) Microcystis et al., 1968). Deep chlorophyll layers involving are encountered in the water column. These motile chrysophytes (E, U:Picket al., 1984; Bird are observed to form striking lee-shore scums and Kalff, 1989), non-motile chlorococcals (X1: in quiet weather (Nakamura and Chang, 2001; Gasol and Pedros-Ali´ o,´ 1991)and picoplankton Ishikawa et al., 2003). Rod-like picoplanktic syne- (Z:Gervaiset al., 1997)tend to be rather more chococcoids (0.4–1.5 µm) become numerous in diffuse. summer (reportedly, up to 106 cells mL−1: Maeda, 1993). Close interval sampling after a typhoon Phytoplankton of sub-Arctic lakes suggested that microplanktic dynamics respond Based on his earlier investigations in the arctic much more to hydrodynamic variability than do and sub-Arctic regions of Sweden and Canada picoplankton numbers (Frenette et al., 1996). (Holmgren, 1968;Schindler and Holmgren, 1971), To conclude the section, the seasonal patterns and on a careful review of the literature, Stef- in the phytoplankton of small nutrient-deficient fanHolmgren devised a systematic and long-term lakes in temperate regions involve oligotrophic experimental study of the lakes in the Kuokkel functional groups in the approximate sequence B district of northen Sweden (centred on 68◦ 25 N, ◦ 2 → X2 → E and/or F → U or LO → N;picoplank- 18 30 E). These lakes are small (0.01–0.03 km ), tic group Z is often an important component. shallow (mean depth 1–6 m) and soft-watered, In the more alkaline waters, E and U are sub- are ice-covered for up to nine months per year stantially missing and more eutrophic (carbon- and, at times, experience 24-h nights (December– concentrating) functional groups C, LM and P are January) and 24-h days (June–July). In the natu- better represented than B, LO and N. ral condition, the lakes are oligotrophic (TP <9 A common feature of stratifying oligotrophic mgPm−2, DIN <240 mg N m−2)butHolmgren’s lakes is the tendency for phytoplankton to form enrichment experiments (+P, +N and +N+P) deep chlorophyll layers. These are not just the raised levels selectively to up to 300 mg P m−2 and consequence of sinking and formation depends DIN to upto6gNm−2.Amongthemany inter- upon algae being able to self-regulate their ver- esting findings he reported (Holmgren, 1983)is tical position, either through their own motil- aproposed ecological classification of arctic–sub- ity or by regulation of their density. Reynolds Arctic phytoplankton (Table 7.2). This recognised (1992c)surmised that their maintenance is gener- the ubiquity of Chrysophyceae and the differing ally conditional upon low diffusivity (they have to matches with other algae, signifying between- be below the epilimnion) and adequate light pen- lake and seasonal variability. Biomass varied with etration (they have to be within the range of net nutrient fertility, being well correlated to N; wind photosynthetic gain or, at worst, balance. The sta- wasabigger influence on seasonality than either tion also offers advantage over a position higher temperature or insolation. Greater water hardin the light gradient and, usually, it is access to nesses supported more diatoms (Urosolenia, Syne- nutrients. The likely algal components are also dra)andcryptophytes. Increased nitrogen lev- influenced by the trophic state and growth con- els promoted Uroglena and the small phagotro- ditions prior to stratification. The size of the lake hic dinoflagellate Gymnodinium.Simultaneously and relative remoteness of the metalimnion from elevated availabilities of higher phosphorus and the surface also affect the physical tenability of nitrogen favoured Chromulina, Ochromonas and the thestructural layers. Among the ‘tightest’, plate- green alga Choricystis.Inallfertilised systems like layers are constructed by photobacteria (V) chlorococcal green alga developed. SPECIES COMPOSITION AND TEMPORAL CHANGE 329

Ta b l e 7.2 Phytoplankton assemblages in Arctic and sub-Arctic lakes, according to the scheme of Holmgren (1983) but using the identiﬁers proposed by Reynolds et al.(2002)

Spring Summer Autumn 1. Chrysophyceae lakes X3, E, Y E 2. Chrysophyceae–diatom lakes X2, X3,E,Y A,(B?) A,Y, LO 3. Chrysophyceae–Cryptophyceae lakes X2, X3, E B, Y B,Y 4. Chrysophyceae–Dinophyceae lakes YU,B,F,LO LO

Phytoplankton in selected regions: in terms of a few key dominant species and medium-sized glacial lakes of the their phylogenetic groups. These patterns were European Alps further distilled by Reynolds et al.(2002) who Besides distinguishing patterns from a selection ascribed Sommer’s (1986)key species to their rel- of particular lake types, it is also helpful to make evant trait-differentiated functional groups (see comparisons of phytoplankton periodicity among also Table 7.3). In this way, (A-group) diatoms regional series of water bodies. Here, between- of the Cyclotella bodanica – C. glomerata group lake differences owe relatively more to edaphic dominated the sparse spring bloom in the olig- distinctions among the individual lake basins otrophic Konigsee¨ (area 5.2 km2,mean depth 98 (and their hydrology, hydrography and hydro- m, TP 5 µgPL−1); in Attersee (area 46 km2, chemistry) than to the general commonality of mean depth 84 m, TP 5 µgPL−1), Tabellaria location or of formation. Regional clustering is species were relatively more prominent. Aulaco- exemplified well by the residual water bodies seira species and Asterionella were abundant in in upland areas where recent glaciations have the mesotrophic lakes, such as Vierwaldstattersee¨ scoured out the typically linear basins of ribbon (area 114 km2,mean depth 104 m, TP 20 µgP lakes or finger lakes. As a generality, these lakes L−1)andAmmersee (area 48 km2, mean depth are usually oligotrophic or mesotrophic in char- 38 m, TP 55 µgPL−1), with increasing subdom- acter. However, it is often also true that the indi- inance of (Y-group) cryptomonads but (D-group) vidual lakes of a given cluster can be ordered Stephanodiscus in the richer waters of Bodensee by productivity or mean biomass supported, or (area 500 km2,mean depth 100 m, TP (then) by typical composition and abundance of phyto- 100 µgPL−1) and Lac Léman (area 582 km2, plankton. Such arrangements are usually illus- mean depth 153 m, TP (then) 80 µgPL−1). The trative of the selective effects on the assembly onset of thermal stratification marked the end of planktic communities within the respective of the spring diatom bloom and, because surviv- regions. ing cryptomonads are always vulnerable to devel- Sommer (1986)undertook such a comparison oping filter-feeding populations of Cladocera, a of the phytoplankton of the deep lakes in the phase of high water clarity ensues. This ‘vacuum’ European Alps. He ably demonstrated a similar- is filled by a summer assemblage whose composi- ity in the year-to-year behaviours in individual tion is particularly sensitive to physico-chemical lakes as well as sequential seasonal stages (spring conditions. Continued bioavailability of phospho- bloom, summer stratification, summer–autumn rusinthe upper water column supports the phase of mixed-layer deepening) common to all growth of CS-strategist algae such as Pandorina of them. He suggested that the different phyto- morum (G-group of motile chlorophytes) and/or plankton assemblages reflected between-lake dif- Anabaena species (H1-group of self-regulating and ferences in trophic status and the availabilities potentially nitrogen-fixing Cyanobacteria). Even- of limiting nutrients, and which were also sen- tual phosphorus depletion is generally marked sitive to between-year variability in individual by increasingly motile (LM-group Ceratium)and lakes. Sommer reported the periodic patterns mixotrophic (E-group Dinobryon)algae,and the 330 COMMUNITY ASSEMBLY IN THE PLANKTON

Ta b l e 7.3 Seasonality of dominant phytoplankton in nine lakes of the European Alps, according to Sommer (1986) but rendered in terms of the trait-differentiated functional groups of Reynolds et al.(2002) (see also Table 7.1)

Spring Clear Summer Summer Summer Late bloom water P↑ Si↑ P↓ Si↑ P↓ Si↓ summer Autumn Königsee AN/YA Attersee NYB Walensee NN/Y Vierwaldstättersee B/YNNHR Lago Maggiore C/RY P L/RH L/R Ammersee C/RY R/P/YP L H R/P Zürichsee C/D/YY Y/HP/YR/P Lac Léman C/D/YY Y/GP L H T/P Bodensee C/D/YY Y/GP L/H/ET/P

development of deep chlorophyll maxima, dom- B grouping. Tabellaria (N) has a long temporal inated by (R-group) Planktothrix rubescens.Onthe period (late autumn – spring) in Lago Maggiore other hand, deeper mixing in summer may sup- (area 213 km2,meandepth176m,TP≤12 µgP port the growthofsummerdiatomsoftheN- L−1)andFragilaria and Aulacoseira granulata are (Tabellaria)andP-(Fragilaria, Aulacoseira granu- frequent throughout the year in Lago di Garda lata)groups, so long as soluble reactive silicon (area 368 km2,mean depth 133 m, TP ∼20 µgP remains available, with the appropriate desmids L−1), Lago d’Iseo (area 62 km2,meandepth122 being more common if it does not. Indeed, nitro- m, TP ≤68 µgPL−1) and Lago di Como (area 146 gen limitation may develop in these instances, km2,mean depth 154 m, TP ≤38 µgPL−1). P- when H-group nitrogen-fixers (Anabaena, Apha- group desmids (notably Closterium aciculare)andT- nizomenon)become active. Autumnal mixing in group filamentous forms (Mougeotia spp.) are also deep lakes enhances the effect of shortening common in these three lakes. Cryptomonas species days in imposing increasingly severe light limi- (Y group) are common throughout the vegetative tation, favouring, in some instances, abundance period in all the lakes; X2-group nanoplankters of (group-T)filamentous chlorophytes and, espe- (Chrysochromulina, Ochromonas, Plagioselmis) occur cially, Mougeotia. in summer, and E-group Dinobryon, LM-group The classification broadly holds for the mildly Ceratium–Gomphospaeria and stratifying R-group alkaline (0.7–2.0 meq L−1), subalpine Italian lakes Planktothrix rubescens are prominent in all the (including Lago di Garda, according to Salmaso lakes during summer. Uroglena species (group U) (2000), and Lago Maggiore, featured in Table 7.3). occur in Lago di Lugano (area 28 km2,mean In a recent synthesis, Salmaso et al.(2003)anal- depth 167 m, TP ≤172 µgPL−1), Lago Maggiore ysed the structure of the phytoplankton in five and Lago di Como. of these lakes. They used different methods from Sommer (1986)and, in consequence, subdivided Phytoplankton in selected regions: small the vegetative season in a different way but the glacial lakes of the English Lake District regional similarities are remarkable. The main Fewlakes have been studied so intensively in features are summarised in Table 7.4 by reference frequency or so extensively through time as to the functional groups of Reynolds et al.(2002). those of the Lake District of north-west England. Diatoms prominent in the early part of the year Time series, starting in some instances in the in all five lakes include Aulacoseira islandica and 1930s, attesting to variable degrees of change Asterionella formosa,representing a mesotrophic attributable to eutrophication (Lund, 1970, 1972; SPECIES COMPOSITION AND TEMPORAL CHANGE 331

Ta b l e 7.4 Summary of phytoplankton seasonality in ﬁve deep subalpine lakes, according to Salmaso et al. (2003) but rendered in terms of the trait-differentiated functional-groups of Reynolds et al.(2002) (see also Table 7.1)

Late winter to Late spring Early mid Late summer – mid spring summer mid autumn Lago di Garda, B, C, P, T, Y Y,P,X2 Y,P,R,T,E,H, Y, P, R, S Lago d’Iseo X2 Lago di Como B, C, N, P, T, Y Y,P,L,U,X2 Y,P,R,T,E,U, Y, P, R H, X2 Lago Maggiore, B, C, N, Y Y, P,L,U,X2 Y,P,R,E,U,H, Y, P, R Lago di Lugano X2

Talling and Heaney, 1988;Kadiri and Reynolds, than silicon or carbon. Nanoplankton is sparse 1993), are now being analysed for sensitivity to (Gorham et al., 1974;Kadiri and Reynolds, 1993). climatic variation (George, 2002). The lakes them- Picoplanktic Cyanobacteria survive the rarefied selves are small, glacial ribbon lakes radiating resource availability in the summer epilimnion, from a central dome of hard, metamorphic slates, where they may form a significant, if not domi- excavating the valleys of a pre-existing radial nant, fraction of the biomass (Hawley and Whit- drainage. The natural vegetation is temperate ton, 1991), while Peridinium willei and small num- Quercus forest but this has been mostly cleared bers of Ceratium may ‘glean’ (sensu the usage for pasture. The lakes themselves are univer- on p. 327)from deeper water. Desmids of the sally soft-watered (alkalinity ≤0.4; most are <0.2 genera Cosmarium and Staurodesmus (group N) meq L−1). Variation among their characteristics are also prominent among the otherwise sparse is dominated by differences in morphometry, ori- microplankton. entation, hydraulic flushing and catchment load- Derwent Water, Coniston Water and Hawes ings of nutrients. They were first arranged in Water are classically mesotrophic. Besides the aseries of ascending ‘productivity’ by Pearsall same A-group diatoms, the spring phytoplankton (1921), which template has been used to illumi- of these lakes may support rather larger quan- nate comparisons of the solute concentrations, tities of Aulacoseira sub-Arctica, Cyclotella praeteris- gross planktic photosynthesis, microbial activity sima (both considered typical of Group B), as and invertebrate associations of the lakes (for fur- well as Asterionella formosa which also appears in ther details, see Sutcliffe et al., 1982;Kadiri and Group C (Table 7.1). Nanoplanktic species (includ- Reynolds, 1993). ing Plagioselmis, Chrysochromulina, Ochromonas,rep- Between-lake differences in the phytoplank- resenting Group X2)arealso quite numerous ton havebeeninvestigatedand reported by Lund in these lakes and may persist (and flourish) (1957), Gorham et al.(1974)andKadiri and for some time after the onset of stratifica- Reynolds (1993). Based on extrapolations made tion. However, the dominant late-spring/early- in these works, it is reasonably easy to deduce summer plankters in these lakes are typically general summaries of phytoplankton periodicity non-motile colonial green algae (Coenochloris fot- in these lakes (see Table 7.5). Among the olig- tii, Dictyosphaerium pulchellum, Pseudosphaerocystis otrophic lakes, the supply of MRP rarely exceeds lacustris, Botryococcus braunii, Paulschulzia pseudo- 1or2µgPL−1 and may remain below detection volvox,Radiococcus plantonicus are among the com- limits for months on end. Chlorophyll concentra- monly observed species) of Group F and/or such tions are also substantially <5 µgchla L−1.Group- colonial chrysophytes as Dinobryon divergens, D. A diatoms, such as Cyclotella comensis, C. radiosa sertularia, D. bavaricum, D. cylindrica, Mallomonas and Urosolenia eriensis,exhaust phosphorus rather caudata and Synura uvella representing group 332 COMMUNITY ASSEMBLY IN THE PLANKTON

Ta b l e 7.5 Summary of phytoplankton seasonality in 19 stratifying lakes in the English Lake District, according to Kadiri and Reynolds (1993), rendered in terms of the trait-differentiated functional-groups of Reynolds et al.(2002) (see also Table 7.1)

TP, c.1991 Class Lake Area (km2)(µgPL−1)Phytoplankton

Larger oligotrophic Wast Water, 0.9–3.0 3–9 A → Z/LO → N lakes Ennerdale Water, Thirlmere, Crummock Water, Buttermere Larger mesotrophic Derwent Water, 3.9–5.4 7–11 B(C) → X2/F/E → lakes Hawes Water, X3/Z/LO/Y → N/R Coniston Water Well-ﬂushed Brothers Water, Rydal 0.2–5.3 4–33 B or C → X1/X2 → short-retention Water, Grasmere, Y (E, F, H2, P) lakes Bassenthwaite Lake Eutrophied larger lakes Windermere (North), 0.6–9.0 14–40 C(B) Ullswater, →X1/X2/Y/G→ Windermere H/LM/S/T → P (South), Esthwaite Water, Lowes Water Enriched small lakes Loughrigg Tarn, ≤0.1 20–45 C/Y → X1/X2 /E/F Blelham Tarn or H1 → LM → P/S

E.Insummer,thebiomassgenerallyfallsto thephytoplankton stimulated by late-summer aphosphorus-depleted minimum during which and autumnal mixing. Phytoplankton biomass is the nanoplankton diversifies with algae such as faintly diacmic in these lakes, the spring peak Chrysococcus, Monochrysis, Pseudopedinella, Bicosoeca (in the order of 6–15 µgchla L−1)usually being tubiformis and Koliella longiseta recruiting (from the larger. The level of MRP generally falls below X3). Picoplankton may also be numerous, some of detection limits for between four (May–August) which may well be Chroococcoid (Z)butsome is and nine (March–November) months of the year. eukaryotic (including Chlorella minutissima, which The summary notation shown in Table 7.5 for Reynolds et al.(2002)placedinX3. These lakes ‘larger mesotrophic lakes’ also fits well to the pat- have the potential to support metalimnetic max- ternsamong the greatest Scottish lochs (Bailey- ima of(group-R) Planktothrix,although the num- Watts and Duncan, 1981). bers of P. mougeotii produced are generally small. Several further lakes are, to varying extents, Cyanobacteria are mainly represented by mod- enriched beyond the mesotrophic state. Since the est growths of Anabaena solitaria and A. lemmer- mid-1960s, Windermere and Ullswater have been mannii (of group H2)andbycolonies of Woroni- subject to the discharge of effluents from sec- chinia (formerly Gomphosphaeria)that, together ondary sewage-treatment works. Esthwaite Water with dinoflagellates Peridinium willei, P. incon- was already a eutrophic lake before sewage treat- spicuum and Ceratium species, represent group LO. ment affected its waters. Lowes Water has a Tabellaria flocculosa and Cosmarium species (includ- low human population in its catchment and ing C. abbreviatum and C. contractum)makeup the reason for its enrichment is not resolved. SPECIES COMPOSITION AND TEMPORAL CHANGE 333

All these lakes can support significant num- South Basin has returned to being dominated by bers of(H1-group) Anabaena flos-aquae, Aphan- P-group diatoms (especially Fragilaria crotonensis) izomenon flos-aquae and, in the case of Esthwaite and desmids (Staurastrum pingue) Water, LM-group Microcystis aeruginosa (together, Before 1992, peak chlorophyll concentrations the bloom-forming Cyanobacteria that have done in the North Basin had come close to 20 µg locally much to give eutrophication its bad chla L−1,inthe enriched South Basin, Tychonema name). Each may also support an abundant populations had forced a summer maximum of nanoplankton in late spring, that may include up to 45 µgchla L−1 and a distinctly diacmic species of Ankyra, Chlorella, Chlamydomonas, Mono- annual pattern of phytoplankton abundance. raphidium, Mallomonas akrokomos (of Group X1) Subsequently, phosphorus load reductions have in addition to X2 representatives, at least until restored the earlier pattern of a spring maximum grazed down by filter-feeders. followed by irregular, smaller summer peaks, all The phytoplankton response to enrichment constrained within the supportive capacity of the (and to the post-1992 restoration) of Windermere biologically available phosphorus. The illustra- has been reviewed and summarised in Reynolds tion in Fig. 7.6 shows the periodicity of chloro- and Irish (2000). Between 1965 and 1991, the phyll concentration in North Basin during 1978. winter maximum of MRP rose from about 2 to Table 7.5 carries entries in respect of two about 8 µgPL−1 in the larger North Basin and smaller Lake District lakes that carry effects from 2.5 to almost 30 µgPL−1 in the South of recent changes in agricultural and domes- Basin. The greater resource has permitted the tic P loadings. In Blelham Tarn, a long-standing vernal diatom growth to escape the rate con- basic B → E/F → LM → N sequence has been trol imposed by phosphorus and to ascend to the steadily altered by the diminution of the con- silicon-determined maximum up to one month tributions of Aulacoseira subarctica, Dinobryon, Cer- earlier (Reynolds, 1997b)(seealsoSection 5.5.2 atium and Tabellaria flocculosa in favour of Asteri- and Fig. 5.13). More than that, from the early onella and Stephanodiscus minutulus (more strongly 1980s, vernal growth in the South Basin often C), several species of Anabaena (H1)species and failed to exhaust the MRP in the lake, leav- anear year-round abundance of Planktothrix ing resource to support enhanced early summer agardhii (S1). production. Grazing by filter-feeders and carbon Finally, several of the lakes have extensive dioxide depletion in the unbuffered water biasses catchment areas in relation to lake volume and, the outcome in favour of the larger, efficient in this area of high annual aggregate precipita- carbon-concentrating bloom-forming Cyanobac- tion (between 1.5 and 4 m annually), are liable teria. Inroads into the DIN stocks has fur- to fairly frequent episodes of significant flush- ther favoured (H1-group) Anabaena species, with, ing. In the case of Grasmere (mean retention appropriately, high incidences of nitrogen-fixing time 24 d, range of instantaneous rates 5–2000 heterocysts. However, the most successful benefi- d), flushing has helped to dissipate the effects of ciary of the eutrophication of the South Basin nutrient loads from sewage works commissioned of Windermere has been the solitary, filamen- in 1969. Thitherto, the lake supported a simi- tous, group-S1 oscillatorian Tychonema bourrellyi. lar assemblage to that of the contemporaneous This particular species lacks gas vesicles and Blelham Tarn, save that the slow-growing algae does slowly sink out to the bottom of the lake of the LM group were (and remain) poorly rep- (thus exporting more oxygen-demanding reduced resented (Reynolds and Lund, 1988). The reason carbon to depth where significant anoxia trig- forthis is not that the algae have difficulty in gered changes in the lake’s metabolism: Heaney growing against the instantaneous rates of flush- et al., 1996). One mark of the success of the ing but that the autumn flooding is so effective programme of tertiary treatment of Winder- in removing pre-encystment vegetative stocks. In mere’s main sewage inputs has been the near- an effort to prevent massive algal growth in dry elimination of Tychonema from the lake. The summer weather, the arrangements for effluent late-summer phytoplankton in Windermere’s disposal were altered in 1982 so that the treated 334 COMMUNITY ASSEMBLY IN THE PLANKTON

liquor was piped to the hypolimnion directly. the oligotrophic tarns and pools in Grasmere’s This admirable interim solution ‘locked’ the sum- catchment. With minimal grazing pressure, large mer phosphorus load in store until the autum- populations of nanoplankton (over 105 cells mL−1 nal breakdown of stratification and the onset of in some instances: Reynolds and Lund, 1988,and rapid hydraulic throughput, washing the phos- authors unpublished observations) develop in phorus harmlessly from the lake. ‘Harmless’ to thephysico-chemically favourable environment. Grasmere, that is, for the phosphorus is moved These soon support correspondingly large pop- through a second, short-retention lake (Rydal ulations of ciliates and rotifers. A quasi-stable Water) to become part of the load to the relatively nanoplanktic biomass of about 0.5 mg C L−1 long-retention Windermere. ‘Harmlessness’ must and a similar biomass of microplanktic con- also be judged in a temporal context: a chronic sumers make an unusual sight for a limnologist! problem arising from infiltration by urban run- Such associations are, however, quite transient. off during wet weather creates large volumes of Ageneration or two of Daphnia galeata recruit- dilute sewage, which is impossible to store pend- ment is eventually capable of clearing the entire ing any kind of treatment. It is normal practice nanoplanktic resource base from the water (and in urban sewage works discharging to rivers to a lot of the ciliates too!). allow incompletely treated effluent into storm One further point of interest that emerges flows where the biological oxidation of resid- from Table 7.5 concerns the larger cryptomonads ual organic carbon is completed naturally. In of group Y.Because the ubiquity of such com- Grasmere, this residual carbon was being piped mon species of Cryptomonas as C. ovata, C. erosa directly to, and collected in, the hypolimnion. and C. marssoni,thereisatendencytooverlook What happened, of course, was a shift in deep- their value in comparing assemblages. They also water metabolism, hypolimetic anoxia and low share features of each of the three, primary C, redox. As this is being written, a further upgrad- R and S strategies in being colonist, in adapting of the sewage-treatment works is in hand. It ing well to low insolation and in their ability could be argued that the real solution (though to constitute deep monospecific plate-like lay- expensive and disruptive) would betore-sewer ers in the metalimnion of stratified lakes. How- our towns so that foul- and surface-drainage are ever, their weakness is to be highly susceptible kept completely separate, with only the former to grazing, by cladocerans, calanoids and cer- needing to be submitted to treatment. tain rotifers (Reynolds, 1995a). In the English In the meantime, the open water of Gras- Lake District, their numbers are broadly propor- mere represents a highly variable environment tional to trophic state: they are sparse in the olig- for phytoplankton. Flushing episodes, especially otrophic lakes (<10 mL−1); collectively, they may during winter, are extremely effective at remov- achieve 10–100 mL−1 in the mesotrophic lakes ing existing algal stocks from the water (ben- and 100–2000 mL−1 in the eutrophic examples. thic propagules are substantially spared). They Moreover, the periods of their abundance occur also deplete the crustacean zooplankton and it progressively earlier in the year with increasing sometimes takes many months for a significant trophic state. This may be due to the interaction feeding pressure to be recovered. What tends of growth potential and the nature and tempo- to happen after a wet winter or spring is that ralphasing of phagotrophy: more nutrients nur- the water column is repopulated from meagre ture the development of larger populations that residual stocks of fast-growing algae (which cer- are detectable sooner (but are also exploited by tainly include C and P groups ofdiatoms, X1- zooplankton earlier). An alternative view is that group nanoplankters and, in Grasmere, Dinobryon the CR qualities of cryptomonad survival strate- spp. which develop striking populations of many- gies are expressed more strongly than the SR celled colonies). Typically, however, X2 and even traits with increasing trophic state. Among the X3 nanoplankters are prominent first. Like other richer Lake District lakes, a small dinoflagellate, rarities (chrysophytes, desmids), some of these formerly recorded as Glenodinium sp. (but now are believed to be brought in by flood waters from recognised as Peridinium lomnickii)iscommon and SPECIES COMPOSITION AND TEMPORAL CHANGE 335 its dynamics coincide sufficiently closely with considered, Carrilaufquen Grande (area 16 km2, those of the spring Cryptomonas that it has been mean depth 3 m, TP 298 µgPL−1)andCarri- included in the spring Y-association (Table 7.1). laufquen Chica (area 5 km2,mean depth 2 m, TP 69 µgPL−1)werethesealgae dominant and Phytoplankton in selected regions: glacial actively fixing nitrogen (Diaz et al., 2000). lakes of Araucania Elsewhere, the lakes are steadfastly olig- Thirty-six north Patagonian lakes, situated on otrophic or slightly mesotrophic in character. either side of the Andean Cordillera between It has to be recognised that the character is ◦ ◦ thelatitudes 39 and 42 S, were the subject of a independent of the most remarkable feature of careful survey carried out over 40 years ago by the region, which is the behaviour of west–east Thomasson (1963). Though not as detailed as passing rain-bearing airstreams. Within a dis- some of the other reports featured in this chap- tance of 50–70 km from the Pacific seaboard, the ter, its inclusion is urged because the striking land rises to the crest of the granitic Andean oligotrophy of the lakes in this region is gener- Cordillera (average altitude about 2000 m, with ally regulated by nitrogen availability (Soto et al., peaks – several of which are volcanoes – of up 1994;Diaz and Pedrozo, 1996). Indeed, the molec- to 3800 m a.s.l.). Progressing a further 60–100 ular N : P ratios to be inferred from the data of km eastwards, the range falls to the level of Diaz et al.(2000)onDINandTPlevelsmeasured theArgentinian plateau, at an altitude of ∼1000 in samples from several lakes on the eastern m a.s.l. Precipitation in the mountains amounts (Argentinian) side of the Andes range between to ∼4mannually but tapers off abruptly to 0.4 and 1.0 (far below 16, reckoned to repre- barely 50 mm. The region is little affected by sent parity). Yet more interesting is the fact that human settlement and a natural vegetation per- maximum phytoplankton biomass observed in a sists over much of the area, in distinct bands number of these lakes correlates well with nitro- corresponding to altitude and rainfall. The high- gen concentration while it is even saturated by est rainforests are dominated by Fitzroya. These MRP, excess of which remains measurable in lake give way to Australocedrus–Nothofagus woodlands. water. From data in Diaz et al.(2000), it is clear Further to the east, this thins steadily, merg- − that in lakes where TP exceeded 11 µgPl 1 (most ing into Agrostis–Cortaderia grasslands (pampas) − values falling between 4 and 8 µgPl 1), the levels and, within 100 km from the Cordillera, to of nitrate + ammonium nitrogen were relatively Festuca–Mulinum. This is surely one of the world’s low. Almost everywhere, DIN levels were <30 µg most remarkable climatic ecotones. Our interest − − NL 1,generally, they were <14 µgNL 1 and, in is that most of the drainage to the lakes emanates − some cases, <3 µgNL 1 (i.e. in the range 0.2–1 from the mountains, flowing westwards in short µMinwhich most phytoplankton are expected to rivers to the Pacific Ocean or eastwards into the experience difficulties harvesting sufficient nitro- Rio Negro catchment that opens to the Atlantic. gen tosupportfurther growth; see Section 5.4.4). The waters in the Araucanian lakes are thus What is of particular interest is that the spare almost uniformly dilute in salts, low in alka- phosphorus capacity seems not to be switched linity and weak in nutrients. The lake waters to the support of nitrogen-fixing Cyanobacteria. are extremely clear (for photosynthetically active −1 Either the phosphorus is still too low (cf. Stewart wavelengths, εmin is between 0.12 to 0.2 m ), and Alexander, 1971), or there is a critical defi- except those charged with fine material emanat- ciency in molybdenum, vanadium or iron (Rueter ing from glacial melt or from the dust of recent and Petersen, 1987), or the energy thresholds for local volcanic eruptions. nitrogen fixation are unsatisfied (Paerl, 1988)(see The phytoplankton assemblages represented Section 4.4.3). Anabaena species are recorded in among these lakes also show a high degree of several ofthelakesandAnabaena solitaria (of the mutual similarity. According to Thomasson’s ‘mesotrophic’ H2 group) occurs widely among (1963)survey and the later information of Diaz et the region’s lakes. However, only in the small al.(2000), the most ubiquitous species recorded steppe lakes, on the eastern fringes of the region have been the diatoms Urosolenia eriensis (group 336 COMMUNITY ASSEMBLY IN THE PLANKTON

A)andAulacoseira granulata (group P; Thomasson also noted the relative abundance of Aphanocapsa also distinguished ‘Melosira hustedtii’),dinoflagel- species, with Staurastrum species and Aulacoseira lates of the genus Gymnodinium and Peridinium in Lago Lacar (area 52 km2). (variously including P. willei, P. bipes,P.volzii, It seems probable that, overall, the phy- P. inconspicuum;presumedtobegroupLO), the toplankton of the Araucanian lakes, with its chrysophyte Dinobryon divergens (group E)andthe basic A/P → E/LO → N or embellished A/P desmid Staurodesmus triangularis (group N). No →X2/F/E/LO → N/P and A/P →E/LO/H2 → information is to hand on the abundance and N/T sequences, conforms to the model of pat- composition of the picoplankton but a presence tern forultraoligotrophic to mesotrophic lakes. as part of a developed microbial food web may In this context, it is interesting that ‘oligotrophic’ be inferred from Thomasson’s (1963)lists of is just as ‘oligotrophic’, regardless of whether planktic ciliates and crustaceans (in which the nitrogen or phosphorus is the main constrain- centropagid calanoid Boeckella gracilipes is a ing factor. The assemblages are, in reality, typi- prominent component). In several lakes, such cal of low-alkalinity systems, although some sup- as Llanquihue (area 851 km2), Ranco (408 km2) posedly more ‘eutrophic’ species, thought to be and Todos Los Santos (181 km2)onthewestern poorly tolerant of low phosphorus conditions side (Thomasson, 1963)and Traful (area 75 km2, (not least Aulacoseira granulata, Fragilaria crotonen- maximum depth >100 m,TP8µgPL−1,DIN∼3 sis and Anabaena spp.), are here able to function µgNL−1)andEspejo (area 38 km2,maxinum adequately. depth >100 m, TP 8 µgPL−1,DIN∼11 µgN L−1)totheeast (Diaz et al., 2000), these are also Phytoplankton of small kataglacial lakes the principal species. So far as it is possible to Wherever glaciers are, or have been in the deduce from limited sampling frequencies, max- last 100 ka, active in eroding terrestrial land- imum biomass occurs in a single summer ‘peak’, forms, there are usually to be found signif- rarely achieving asmuchas1µgchla L−1.An icant ‘downstream’ deposits of directly trans- ubiquitous nanoplanktic (X2 group) component ported material, abandoned by the wasting (Plagioselmis, Chrysochromulina)isweaklyexpressed glaciers (hence ‘kataglacial’). Associated forma- in these ultraoligotrophic systems. Elsewhere, tions caused by ‘freeze-thaw’ cycles and solifluc- the same species may achieve larger standing tion in the vicinity of ice fields are known crops and where which the presence of other collectively as periglacial deposits. Depending species may be more evident. In Lago Villarrica upon their age, morphometry and the contempo- (area 851 km2), Thomasson (1963)notedasignifi- rary climatic conditions, these deposits may well cant (F group) representation of Kirchneriella and enclose small lake basins. In the wake of the most Dictyosphaerium species. The annual cycle in Lago recent glacial period that ended about 10.5 ka Nauel Huapi (area 556 km2, maximum depth ago (known as the Devensian in northern Europe, 464 m, mean depth 157 m, TP 11 µgPL−1, DIN theWeichselian in the European Alps and the ∼10 µgNL−1)movesfromaspring assemblage Wisconsinian in North America), vast terminal- of Aulacoseira–Urosolenia–Dictyosphaerium,through moraine systems were deposited along the south- Dinobryon–Dictyosphaerium–Urosolenia in sum- ern limits of the ice sheets. These abandoned mer to a diatom (Aulacoseira, Urosolenia–Synedra ‘tidemarks’ of characteristically hummocky land- ulna–Tabellaria)-dominated autumn plankton scapes are sometimes called moraine belts. These (Thomasson, 1963). The (summer) chlorophyll kataglacial moraines, peppered with generally maximum is still <2 µgchla L−1 (Diaz et al., small lakes, make up distinctive landscapes in the 2000). Several of the smaller lakes support an vicinity of Riding Mountain, Manitoba and across array of desmids (Cosmarium, Staurastrum spp.), as northern Minnesota and Wisconsin. In Europe, well as Fragilaria crotonensis (P)andMougeotia (T). major moraine belts sweep through Jylland (Jut- Anabaena solitaria (H2)also occurs quite widely; land), Holstein, Pomerania and Mazuria, and it Thomasson recorded it as being dominant in is the morainic system striking north-eastwards autumn in Lago Correntoso (area 26 km2); he across northern Russia that separates the Baltic SPECIES COMPOSITION AND TEMPORAL CHANGE 337 and Black Sea watersheds in that country. The texts show standing surface waters wherever the largest moraines were formed during periods topographic contours dip below the level of the of ice-front stagnation, when and where glacier local water table and, thus, merely its surface recruitment and glacier melt were, for a time, manifestation. Hydrological studies of these drift in approximate equilibrium. In front of them hollows confound this simplicity as annual lake stand massive outwash plains of fluvioglacial levels fluctuate less than does the height of the deposits. Behind them are the lands smoothed water table. Reynolds (1979b)proposedamodel by the advancing ice and plastered with com- in which lake basins were partially sealed by their pacted, ground-down boulder clay, or till, which owndeposits and that ground water entered by may be only lightly and locally covered with ‘inspilling’ from a high water table. Lake water later fluvioglacial deposits. Less expansive but ‘overflows’ normally leak away by seepage. When wholly analogous structures abound in the low- thewater table dropped, hydraulic exchanges land outfalls of valley glaciers and ice sheets in were more or less confined to precipitation and other parts of the world. Those with which I am evaporation from the lake surface. The fact that, most familiar are located in the English north- on millennial timescales, basins have varied in west midlands, especially the Wrexham–Bar Hill their trophic status according to the wetness moraine (Reynolds, 1979b). of past climates, many becoming ‘terrestrialised’ The wane of the Pleistocene ice sheets into fens or peat bogs (Tallis, 1973), also demands wasnever smooth but occurred in phases of amodel of restricted basin permeability. rapid retreat, alternating with phases of stag- Notwithstanding, much of the water supplied nation or even readvance (West, 1977). Lesser to basins in drift has percolated through sub- morainic features are widespread among areas soils and fluvioglacial deposits that are gener- of kataglacial deposition. The variety of struc- ally finely divided, offering maximum contact tures in drift material (which term embraces opportunities for the solution and leaching of all glacial deposits) is increased by proximity to salts. In this way, the chemical composition of solid geological features as well as in the for- lake water is strongly influenced by the local mations themselves, such as kames (ice-deposited drifts. This does not mean that drift lakes are mounds), eskers (englacial stream beds) and pin- necessarily rich in nutrients (many are not: Stech- gos (periglacial frost heaves in drift outside the linsee is one that is quite nutrient-poor; see p. ice fronts). Lake basins indriftsarejust as varied 326)but many certainly are. Moderately to very in the detail of their origins. Some are moraine- calcareous lakes are frequent among kataglacial dammed gaps between drift hummocks and are series (Ca 0.4–4 meq L−1,bicarbonate alkalinities irregular or linear in outline; others are more ≤3.5 meq L−1), though they may be rare locally, rounded with excentric underwater contours, depending upon the provenance of the drift. Sim- corresponding to kettle-holes formed initially by ilarly, with nutrients, the dissolved silicon and the melting of detatched blocks of ice. orthophosphate contents of unmodified ground- However, lakes in kataglacial drifts do have waterare variable from catchment to catchment several generic and crucial common attributes. but may easily reach 7–8 mg Si L−1 and >300 The unconsolidated deposits in which they are µgPL−1 in some instances. Other major ions formed are generally porous, so that present-day may be similarly enriched in particular systems. precipitation percolates into the drift rather than Unless the topographical catchments have been runs over the topographical surface. The water subject to considerable anthropogenic modifica- collects in a zone of saturation above the basal tion, there is little scope for the enrichment of till, which is relatively impervious. The ‘surface’ nitrogen, save through the same surface evapo- of the saturated zone is called the phreatic sur- rative processes that affect all precipitation. This face, or water table, and, again, represents a sort leads to another general attribute of morainic of contemporary equilbrium between its recruit- and drift lakes, that the ratios of biologically ment by percolation and the sluggish horizon- exploitable contents of nitrogen to phosphorus tal permeation into regional catchments. Older and to silicon are lower or much lower than in 338 COMMUNITY ASSEMBLY IN THE PLANKTON

surface-fed water bodies. The capacity of the Transparency is reduced to 2–3 m. Silicon is gen- nitrogen to support algal growth may be less erally heavily drawn down (from ∼2.5 to <0.1 mg than that of phosphorus and algal growth rates Si L−1) while Monoraphidium,othergreen algae in the field are,potentially,morelikelytobelim- and the Y-group cryptophyte Chroomonas persist ited by the external supply of nitrogen than by in the epilimnion (7–10 m in thickness), pend- the phosphorus available. ing the exhaustion of DIN to <5 µgNL−1. The phytoplankton of a number of ground However, available phosphorus remains freely water-fed drift lakes has been described in some available (SRP >150 µgPL−1) and, not surpris- detail. Sjon¨ Erken in Sweden (area 24 km2,mean ingly, nitrogen-fixing H1-group Anabaena species depth 9.0 m, TP 25–50 µgPL−1) has been observed (A. flos-aquae, A. planctonica, A. spiroides) dominate regularly for many years. Rodhe et al.(1958)and through the summer. In autumn, Asterionella, Nauwerck (1963)notedtheApril–May develop- Fragilaria and other diatoms dominate the declin- ment of a spring ‘bloom’ (maximum ∼20 µg ing biomass. Epilimnetic pH in summer rises to chla L−1)offlagellates (including Cryptomonas pH 8.8 or a little higher, with carbonate precipita- spp., Plagioselmis, Chrysochromulina and Dinobryon tion. The X1 → C/Y → H1 → C/P sequence owes divergens), starting under ice cover but soon much to the diminution of nitrogen and carbon giving place to dominant diatoms (including levels during the vegetation season. ‘large’ Stephanodiscus rotula and ‘small’ Stephano- The drift lakes around Plon¨ in North Ger- discus hantzschii var. pusillus and Asterionella form- many also became classic sites in limnology, osa). Green algae (including Eudorina and Pan- especially through the studies of August Thiene- dorina spp.) and Cyanobacteria appeared in the mann. He distinguished their ‘Baltic’ biotic early part of summer (Anabaena flos-aquae, Aphan- assemblages – of benthos as well as of plank- izomenon flos-aquae and, especially, Gloeotrichia ech- ton–from those (‘Caledonian’ assemblages) of inulata)tobereplacedbyGomphosphaeria (now European mountain lakes. The former included Woronichinia)andCeratium hirundinella,building what we now refer to eutrophic diatoms (C, to an August maximum of 30–35 µgchla L−1 D, P associations), cryptomonads, Cyanobacte- (see also Fig. 7.6). With early autumnal mixing, ria and dinoflagellates. Sommer’s (1988c)exper- Fragilaria and Staurastrum species became promi- imental investigation of Schohsee¨ (area 0.79 nent. Now, nearly 50 years later (D. Pierson, per- km2,mean depth ∼9m)demonstrated not just sonal communication), the same floral elements theseasonal progression but, through the use (C/D/X2/Y/E → G/H → LO → P)are encoun- of a series of enrichment bioassays, also the tered but the dominance has changed slightly nutrients most severely constraining contempo- in favour of Stephanodiscus hantzschii var. pusilla, raneous growth capacity. Vernal diatoms (Asteri- nanoplanktic flagellates, summer Gloeotrichia and onella formosa, Synedra acus, Diatoma elongatum, late-summer Asterionella in a sequence closer to Stephanodiscus rotula and S. minutula)were, in (X2/D → H2 → LO → C). most instances Si-limited. The supportive capac- Esrum Sø (area 17.3 km2,meandepth12m) ity for Cyanobacteria (Anabaena flos-aquae)was is a large kettle-hole in calcareous sandy moraine often P-limited, while summer dinoflagellate pop- in Sjælland, Denmark which has, like Erken lake, ulations were sensitive to limiting availabili- along history as a focus for detailed studies ties of nitrogen (Ceratium)orphosphorus (Peri- (recently reviewed, in part, by Jonasson,´ 2003). dinium cinctum, P. umbonatum, P. inconspicuum). The Its phytoplankton, as described by Jonasson´ and growth of (group-F) colonial chlorophytes, (group- Kristiansen (1967)developsduring March under a E)chrysophytes (Dinobryon spp.), cryptomonads thinning ice cover and dominated by nanoplank- (Cyptomonas ovata, Plagioselmis nanoplanctica)and tic Ankistrodesmus falcatus,nowknown as Mono- other nanoplankters (Ankyra judayi, Chrysochromu- raphidium contortum and ascribed by Reynolds et lina parva)was rarely constrained by nutrients al.(2002)togroupX1.Afterice break, domi- but these would, perhaps, have experienced con- nance of the April spring peak passes to diatoms trol through the carbon supply or through graz- (predominantly B/C-group Asterionella formosa). ers or both. The summarised annual sequence SPECIES COMPOSITION AND TEMPORAL CHANGE 339

(C/D/Y → X1/X2/Y/E → H1/F → LM) corre- may persist beyond spring (rarely resorting to sponds to the drawdown of silicon, then nitrogen heterocyst production and nitrogen fixation). Cer- and/or phosphorus, but always against a back- atium or Microcystis usually dominates the sum- ground of frequent carbon dioxide deficiencies. mer biomass (though not, it seems, as a func- In the small calcareous meres of the English tion of nutrient availability but of recruitment north-west midlands, phosphorus availability is success: Reynolds and Bellinger, 1992). P-group generally moderate to high, owing to a relative diatoms or even S1-group Planktothrix agardhii abundance in the drift of minerals derived from have dominated in windy summers and, in the underlying Triassic marls and evaporites. The one recent case, J-group Scenedesmus took over oceanic climate to which these lakes are sub- averyshallowepilimnion during an unusually ject ensures that they are generally ice-free in calm summer (Reynolds and Bellinger, 1992). J- winter (warm monomictic lakes). In Crose Mere group Scenedesmus, Pediastrum and other chloro- (area 0.15 km2,meandepth4.8m, alkalinity coccalean algae are abundant in meres that have 3.2 meq L−1, SRP ≤ 200 µgPL−1;DINgenerally experienced recent enrichment from nitrogen- ≤2mgNL−1), the phytoplankton often achieves rich agricultural fertiliser run-off while some high biomass (150–250 µgchla L−1 in summer) low-alkalinity meres in sandy drift support more in a distinct, diacmic seasonal pattern (see Fig. green algae of the F group (especially Botryococcus 7.6). The basic periodic sequence of the phyto- in Oak Mere: Reynolds, 1979b). plankton (C/Y → G → H1 → LM → P)begins Finally, it may be added that the summary C with a February–March maximum of Asterionella, → H1 → LM → P applies to Mazurian moraine Stephanodiscus rotula and Cryptomonas ovata (which lakes such as Mikolajskie (Kajak et al., 1972)and may, but more usually does not, exhaust the North American prairie lakes (Lin, 1972;Kling, silicon). The onset of thermal stratification (in 1975). late April–early May, to within 2–6 m of the surface) leads to the rapid settlement of the diatoms Phytoplankton of large, low-latitude lakes (see also Fig. 6.2), while surviving nanoplank- The phytoplankton of the great lakes of Africa ters and cryptomonads succumb to intensifying differs markedly from that of the high-latitude grazing rates. Eudorina unicocca,the next dom- examples considered above, but in ways that are inant, mostly escapes grazing but depletes the more easily appreciated in the light of knowl- DIN. By late June, nitrogen-fixing Anabaena circi- edge based on smaller lakes. The lakes themselves nalis and/or Aphanizomenon flos-aquae are propon- differ in character, though most of the African derent but Ceratium hirundinella,together with examples to be mentioned here are of tectonic Microcystis aeruginosa,trawlintothemetalimnion origin, being aligned in the opening and bifur- for the nutrients to sustain the major biomass cating rift across East Africa. Its southern arm peak of the year. Autumn mixing (or earlier sum- encloses Lake Malawi; a string of lakes traces the mer storms) promotes renewed phases of diatom western section, including Lac Tanganyika, Lac abundance (Fragilaria crotonensis, Aulacoseira granu- Kivu and, at the northern end, N’zigi (formerly lata plus the desmid Closterium aciculare). For full Lake Albert and flushed by the upper reaches of details, see Reynolds (1973c, 1976a). the White Nile). The eastern rift valley contains There is some interannual variability about Turkana (formerly Lake Rudolf) as well as several this sequence (see especially Reynolds and smaller lakes. In the plateau between the eastern Reynolds, 1985)butacore C → H1 → LM → and western arms is a water-filled depression of P is common throughout the deeper lakes of aquite different character – the gigantic saucer the series (shallower lakes have less Ceratium and, that is Lake Victoria whose origin is not tectonic sometimes, more Microcystis). In Rostherne Mere and, it is believed, quite recent. (area 0.49 km2,meandepth13.4 m, SRP ≤ 300 The rift valley lakes are ancient (possibly up to µgPL−1,maximum DIN generally 1.5–2 mg N 20 Ma: Coulter, 1994), deep and, because of the L−1), depth and turbidity suppress a spring bloom climate (‘endless summer’: Kilham and Kilham, (unless stratification is delayed). H1 dominance 1990)attheir respective latitudes, almost never 340 COMMUNITY ASSEMBLY IN THE PLANKTON

experience full convectional overturn. Malawi, populations (3–6 × 10−6 L−1)and abundant Tanganyika, Kivu and Turkana are meromictic ciliates (especially Strombidium sp.) are indica- lakes: each is vertically segregated into a peren- tive of an active microbial food web (Hecky nially stagnant, lower monimolimnion and an and Fee, 1981;Heckyet al., 1991; Plisnier and upper mixolimnion. The monimolimnion retains Coenens, 2001). As the windy season abates, algal most of the nutrients in the system but is biomass increases at the northern end, with the severely energy-limited; the mixolimnion is fre- development of Anabaena blooms, while pulsed quently nutrient-deficient (Hecky et al., 1991). upwellings at either end deliver the nutrients Even so, there is strong phytoplankton seasonal- to sustain the main phase of diatom growth ity in these lakes which relates to variability in (Nitzschia spp. and Aulacoseira granulata are promi- thedepth of the mixolimnion through the year. nent), to maximal concentrations of ∼7 µgchla Entrainment of deeper water during the period L−1 (Langenberg et al., 2002). However, as the of increased mixing is extremely important to seiching weakens and the mixolimnetic nutrient the recycling and reuse of some of the system’s base is dissipated in fish production and the sedi- accumulated resources. Otherwise, new produc- mentary flux, it is green algae such as Coenochloris tion in the pelagic relies on the supply of new and Oocystis that persist longest through February resources (Hecky and Kling, 1981). to April (Hecky and Kling, 1981;Talling, 1986). Ataquotedmaximum depth of 1471 m (Her- From the mixing to final relaxation and the next dendorf, 1982), Lac Tanganyika is the second cycle, phytoplankton composition may be sum- deepest lake on the planet (area 32 900 km2, marised as P → F → Z (with the advantage to P mean depth 574 m). Between May and Septem- perhaps alternating with one in favour of H with ber, south-easterly winds are funnelled up the val- the seichecycle). ◦ ley and drive surface water (temperature ∼27 C) In Lake Malawi (area 22 490 km2, mean depth to the north, where the pycnocline may be 276 m), seasonal variations in the depth of the depressed to a depth of ∼70 m (data of Plisnier mixolimnion range from ∼70 m in the cooler, and Coenens, 2001). When the south-east winds windier part of the year (June to September), stop, the tilted surface of the monimolimnion when its temperature falls to ≥24 ◦C(barely more continues to oscillate (or seiches) for several than 1◦ warmer than the monimolimnion), to months until the stability is recovered (gener- <30 m during the hot, calmer months between ally by February). Monimolimnetic water may October and March (temperature >27 ◦C). The be sheared off into the mixolimnion during the major nutrients occur at low concentrations, windy months, while its simultaneous upwelling except at depth (>200 m, in the anoxic moni- at the southern end (and also at the northern molimnion). Mixolimnetic concentrations are at end during the period of oscillation) augments their highest during the mixed periods (SRP ∼5 the process. Between February and April, the µgL−1,DIN∼20 µgL−1: data of Irvine et al., 2001) only source of nutrients to mixolimnetic primary but these are soon drawn down after the winds production is external. The mean mixolimnetic ease. Irvine et al.(2001) observed that planktic nutrient concentrations (0–30 m) are higher (DIN chlorophyll concentrations are typically <2 µg − − 70 µgL 1, SRP 50 µgL 1)intheperiodofwind chla L−1 with higher levels (≤7 µgchla L−1) shearing and upwelling than in the calm period coming during July. Diatoms are prevalent dur- − − (DIN 50 µgL1, SRP 20 µgL1), even though ing the windier months (Aulacoseira granulata, this is also the wet season of enhanced lake Cyclostephanos sp.), with desmid species of Stauras- inflows. trum and Closterium). Nitrogen-fixing Cyanobacte- Phytoplankton biomass increases gradually ria Anabaena and Cylindrospermopsis species make between May and August and progresses from up 50% of the planktic biomass in the months south to north (Hecky and Kling, 1981), from of stable stratification (Allison et al., 1996;Irvine − the equivalent of <1to∼2 µgchla L 1 (data of et al., 2001). These authors give no specific infor- Langenberg et al., 2002). Picoplanktic Cyanobac- mation on either pico- or nanophytoplankton, teria contribute a large (>50%) proportion of the although the latter, at least, are likely to be rel- particulate primary production, while bacterial atively most abundant during the early stages SPECIES COMPOSITION AND TEMPORAL CHANGE 341 of the intensification of the thermal stratifica- primary production and a doubling of the verti- tion. Pending confirmation of this, the phyto- cal coefficient of light attenuation since Talling’s plankton sequences are best summarised as (1965)observations in the 1960s (Mugidde, 1993). P → H1 (SN). The hypolimnion, which was previously aerated The phytoplankton of Lac Kivu (area 2370 to the deepest sediment through most of the km2,meandepth 240 m, TP ≤55 µgPL−1)shows year, is now regularly anoxic. These may be many compositional similarities to that of Lake responses to changes that started earlier than Malawi. The stable part of the temperature gradi- the1950s but they have most certainly acceler- ent (and associated chemocline) begins at about ated since. There is an increasing nutrient load 60 m, which is sufficiently shallow to support originating from the activities (notably urbanisa- awell-developed plate of photosynthetic bacteria tion and erosion consequential on intensifying (Haberyan and Hecky, 1987). Eukaryote produc- agriculture) of a large (∼20 million) and increas- tion in the mixolimnion is greatest following the ing (3–4% a−1) human population resident in the periods of more active mixing, but nanoplank- lake’s catchment. Total phosphorus concentra- ton and,later,the Cyanobacteria Microcystis tions in the lake water (now 45–72 µgPL−1)have and Spirulina species feature with Anabaena and roughly doubled and the area-specific sedimenta- Cylindrospermopsis in the calm period (Serruya and tion rates have gone up by a similar factor (Ram- Pollingher, 1983). By way of summary, P → X → lal et al., 2001). Levels of DIN were, and remain, H1/LM/SN/S2)isprobablyafairrepresentation. low: the nitrogen limitation of production recog- In Lake Turkana (area 8660 km2,meandepth29 nised by Talling (1965)persists. Average silicon m), where mixing involves a much larger propor- levels have fallen considerably. Coincidentally, tion of the lake volume, phosphorus has accumu- the ecosystem has been catastrophically altered −1 lated to high levels (TP 1.8–2.4 mg P L ,[SRP]max by theintroduction during this period of Nile ≤786 µgPL−1:Hopson,1982). The diatom assem- perch (Lates niloticus)and Nile tilapia (Oreochromis blage conspicuously includes ‘large’ species of niloticus) which have expanded at the expense of Surirella and Coscinodiscus; F-group colonial chloro- thelake’s endemic populations of haplochromine phytes appear as stability increases in January cichlids (Ogutu-Ohwayu, 1990;Witte et al., but soon give dominant place to nitrogen-fixing 1992). Anabaena species. Microcystis species also develop The phytoplankton of Lake Victoria in the in some numbers (Liti et al., 1991). The sequence 1960s has been characterised by Talling (1965, is partly captured in the summary notation P → 1986, 1987). Despite the great difference in basin F → H1/LM. morphometry, Lake Victoria was subject to a pat- In contrast to the rift-valley lakes, Lake Vic- tern of alternating dominance between diatoms toria isyoung(possibly as little as 12 000 a) during the mixed periods (especially by what and quite shallow (mean depth 39 m, max- are now referred to as Aulacoseira granulata and imum depth 84 m) in relation to its area Cyclostephanos spp.) and nitrogen-fixers Anabaena (68 800 km2). Like the rift-valley lakes, however, and Anabaenopsis species in the stratified phase. it experiences seasonal alternation between a Also present were Closterium species and a variety warm,wet (October–May) and a cool, dry season of chlorococcal algae associated with enriched (June–September). The lake is wind-mixed to the shallow conditions (Scenedesmus, Pediastrum, Coelas- bottom on frequent occasions during July and trum spp. of group J). Chlorophyll-a concentration August. From the limnological information on in the open lake varied between 1.2 and 5.5 µg thelake that has accumulated since systematic chla L−1,though higher concentrations could be information started to become available (Fish, found in the thermocline. 1952;Talling, 1965;Beadle, 1974), it is quite clear By the 1990s, Aulacoseira had declined to the that changes within and beyond the lake dur- point of rarity and Anabaena, Anabaenopsis and ing the last 40 years have had a profound influ- Aphanizomenon occurred only sporadically (Kling ence upon the biota (Hecky, 1993;Kling et al., et al., 2001). Nitzschia acicularis had become the 2001). These include an eight- to tenfold increase dominant diatom, peaking between September in the phytoplankton chlorophyll, a doubling of and November. This alga is typical of much 342 COMMUNITY ASSEMBLY IN THE PLANKTON

smaller, usually enriched and turbid, bodies of between November and April, to the bottom. In water and some lowland rivers and ascribed by theintermediate quiescent episodes, microstrati- Reynolds et al.(2002)tofunctional group D. fication develops to within a few metres of the Though representing a larger biovolume than all lake surface. Although the absolute and rela- thediatoms together in the 1960s, Nitzschia pro- tive abundances among them may vary among duction in the Lake Victoria of the 1990s was episodes, the responding populations conform to overshadowed by that of Cyanobacteria. Cylindros- aclearand general pattern. Aulacoseira is ususally permopsis now dominated the nitrogen-fixer niche the dominant species among the diatoms that in the stratified period, while solitary, filamen- increase with each mixing event. As the mix- tous non-nitrogen-fixing species of Planktolyngbya ing weakens, cryptomonads briefly replace the had become abundant in the mixed period. The settling diatoms but fall victim to cladoceran former P/J → H1 alternation had been usurped filter-feeding. The clearing, stabilising epilimnion by a D/S1 → SN sequence whose selection is is populated by various colonial green algae, forced presumably by the requirement for supe- by Anabaena and then by migrating peridinoid rior antennal properties. dinoflagellates. In chemical terms, the lake is Brief reference should be made to one or more mesotrophic than eutrophic and deficient two other, well-researched tropical systems out- in nitrogen rather than phosphorus. The sum- side Africa which experience quite different pat- mary sequence P → Y → F → H1 → LM applies ternsofseasonal forcing. Lago Titicaca (area 8559 comfortably to the periodicity of species in many km2,mean depth 107 m, stratified October–July low-latitude lakes including that of another trop- to within 40–70 m of the surface) supports a max- ical lake studied by Lewis (1986), Lago Valencia, imum biomass during the early stages of mixing Venezuela. (May–June, when Aulacoseira and other diatoms are relatively abundant: Richerson et al., 1986; Phytoplankton in shallow lakes Dejoux and Iltis, 1992). SRP levels are ≤23 µg In terms of number, most lakes are absolutely chla L−1,butDINislow(<50 µgNL−1:Vincent small (as defined on p. 325)and,commonly, ‘rel- et al., 1984). Planktic nitrogen fixation is mod- atively shallow’ (as outlined on p. 320). The essen- est, however, and nitrogen deficiency, together tial property of a shallow lake is that much with light dilution, appears to most constrain or all of the bottom sediment surface is fre- production. Diurnal heating and nocturnal cool- quently, if not continuously, contiguous with the ing cause wide daily fluctuations in stability. Few open-water phase of the habitat (Padisak´ and algae accommodate to this diel stratification but Reynolds, 2003). The consequences may be mani- group-F colonial chlorophytes, together with self- fest in any of several ways. Subject to particle size, regulating Peridinium species (LO)arerelatively depth and clarity, the bottom surfaces may sup- tolerant and predominate during this part of the port epilithic algae or rooted macrophytic plants year. (which, sensu lato,include large algae, mosses and Finally, theapparentassociation of diatoms pteridophytes, as well as angiosperms). Finer sed- and solitary filamentous cyanobacteria with iments are liable to entrainment by penetrat- mixed water columns, and (for different reasons) ing turbulence; this may well increase turbid- of rapid-growing flagellates, nitrogen-fixers and ity and light-scattering and, thus, impair light self-regulating gleaners is well demonstrated in penetration. On the other hand, however, the tropical Lake Lanao, the Philippines (area 357 simultaneous entrainment of interstitial water km2,mean depth 60 m). Lewis’ (1978a) penetrat- and biogenic detritus provides a mechanism for ing analysis of phytoplankton periodicity in this the accelerated return of resources back to the lake provides may insights into plankton ecology water column. From the point of view of ecosys- elsewhere. The lake is subject year-round to fre- tem function, the pelagic systems of shallow quent stormyepisodes (10–15 a−1;thebehaviour lakes differ from those of deep lakes and seas is described as atelomictic)that mix the lake in not becoming isolated from a significant store to depths >20 m, sometimes to >40mand, of dead, decomposing biomass. SPECIES COMPOSITION AND TEMPORAL CHANGE 343

On this basis, some ‘large lakes’ (>500 km2, 1993). One is a vegetated state with clear water; at least when they are full of water) are also theother is a potentialy turbid, phytoplankton- ‘shallow’: these include the Lakes Winnipeg, dominated system. Moreover, many cases Balkhash, Tchad, Eyre and Bangweolo (Reynolds together indicate that small lakes can switch et al., 2000). Neither these, nor any of the greatly abruptly between these two stable states (Blindow more numerous small lakes, support a character- et al., 1993:Scheffer, 1998), under the influence of istic or recognisable ‘shallow water phytoplank- switches in the resource–consumer interaction. ton’ – community assembly invokes other crit- Restricting the present discussion to the phy- ical factors. Yet phytoplankton is important to toplankton composition, the structural influ- perceptions of water quality in very many shal- ences in shallow waters fall into several cat- low lakes (Scheffer, 1998), so it is valuable to egories. Phytoplankton may be present in be able to extract some general principles. One small concentrations if bioavailable resources of these is that, in a majority of truly ‘small’ in the water are modest (advantage to rooted (<200 m across) and absolutely ‘shallow’ (≤5m) macrophytes exploiting additional or alternative waterbodies have a theoretical light-supportive resources) or, if not, if macrophytic vegetation capacity of ≤600 mg chla m−2 (say, 30Cm−2), harbours the food web that can exert ongo- unless they are at high latitude or their waters ing controls on the development of phytoplank- are heavily stained with humic substances. This ton. Phytoplankton can dominate in the open provides plenty of scope for the intervention waterabove macrophytes rooted 1–1.5 m below of other potential limiting factors. Interestingly, thewater surface. In temperate waters, they can Scheffer (1998)provided a plot of the average respond earlier and faster than macrophytes to summer chlorophyll-a concentrations in each of lengthening days. If circumstances prevail where 88 shallow lakes in the Netherlands (mean of there is no adequate consumer control, phyto- mean depths 2.1 m) against its average summer plankton have the potential to shade out rooted TP concentration. Up to 0.3 mg P L−1,thepoints benthos or, at least, to contain its distribution to cluster beneath a slope of chla = 0.9 TP. At TP the shallowest margins. concentrations >0.3 mg P L−1,chlorophyll levels Some of the representative shallow-lake phy- show a typical P-saturation response. An analo- toplankton assemblages may be noted. Unicellu- gous dataset for the same lakes shows a similar lar nanoplanktic forms are collectively common, behaviour with respect to TN, with the points benefiting from C-type invasive, fast-growth- clustering beneath a slope of chla = 0.09 (TN – rate strategies. These often include nanoplank- 0.7), up to TN ∼4mgNl−1.However,avery tic chlorococcals (Chlorella, Monoraphidium spp. large number of records apply in systems with of group X1), nanoplanktic flagellates (Chlamydo- markedly lower TP and TN availabilities but, nev- monas, Plagioselmis, Chrysochromulina of group X2) ertheless, show marked saturation of the chloro- and group-Y cryptomonads and small peri- phyll actually supported. dinioids. A polyphyletic group-W1 association of In many of these small lakes, there is a euglenoids (Phacus, Lepocinclis as well as the type complex interaction with rooted, submerged genus, Euglena), chrysophycean (especially Synura plants, which, in these shallow waters, are able spp.) and small volvocalean colonies (especially to compete effectively in energy- and resource- Gonium)mayberepresented. On the basis of a harvesting. The complexities arise through floristic comparison of small, shallow lakes in thebehavioural interactions among benthic Hungary, Padisak´ et al.(2003c)noted the frequent macroinvertebrates, littoral cladoceran zooplank- co-occurrence of Phacotus spp. with this group ton and their respective planktivorous and ben- and its dominance in calcareous waters; they pro- thivorous consumers (including fish) (see Section posed a new group identity in YPH. Larger green 8.3.6). Suffice it to say here that aquatic primary colonies are represented by Volvox, Eudorina and production and its heterotrophic consumers can Pandorina of group G.Colonial chrysophytes (espe- strike quite different and alternative steady states cially Dinobryon spp.) are also abundant in small in shallow lakes (Scheffer, 1989;Schefferet al., waterbodies, even quite calcareous ones, if there 344 COMMUNITY ASSEMBLY IN THE PLANKTON

is an good supply of carbon dioxide (e.g. from Lagerheimia, Closterium and Chlorella by onein benthic decomposition of plant matter, includ- which Asterionella, Pediastrum, Anabaena and even ing fallen leaves). Planktic diatoms are not gen- Microcystis formed successive populations. The erally abundant in the small, shallow ponds save trigger was the introduction of base-rich water for the small Stephanodiscus species, and perhaps from a trial bore that raised the ambient pH of the smaller Synedra species (group D). Gyrosigma, the lake from 4.5 to 6.5 (Swale, 1968;Reynolds Surirella and Melosira varians that are tychoplank- and Allen, 1968). tic, as well as Aulacoseira species that are mero- Abundant populations (perhaps equivalent to planktic (the distinction is actually very fine 100–600 µgchla L−1)ofphytoplankton occur- here), may be prominent in shallow lakes that are ring in small, shallow and continuously nutrient- exposed to wind and wave action (including large rich, hypertrophic lakes and in which, through lakes such as Balkhash and Tchad). Elsewhere, trophic imbalances, heavy grazing by zooplank- B, C, N and P groups of diatoms and desmids ton is avoided, frequently comprise species of are common, provided their suspension require- Scenedesmus, Coelastrum and Pediastrum (group ments are fulfilled by the absolute water-column J), often with X1-group nanoplankters such depth (see Sections 2.6.2, 6.3.2)insmalllakes. as Chlorella, Ankyra and/or Monoraphidium. The The diatoms remain sensitive to silicon exhaus- assemblage is well represented in the phyto- tion and they may be replaced by other algae, plankton of habitats where high nutrient load- including non-vacuolate, small-celled blue-green ing is equated with high hydraulic loads and in their colonial phases (Aphanocapsa, Aphanoth- rapid flushing rates that discount against slow- ece of group K)orbynon-motile colonies of growing algae and most species of mesozooplank- group-F green algae, such as Botryococcus.Inshal- ton. These include hypertrophic rivers, some low lake Sniardwy,´ Poland (area 110 km2,mean flood-plain lakes flushed by river flow, natural depth 5.9 m), Aulacoseira species alternate with ponds enriched with sewage and many artificial group-J Scenedesmus and Pediastrum species (Kajak ponds constructed to bring about its oxidation et al., 1972). During the 1970s, a similar assem- (Uhlmann, 1971;Boucher et al., 1984; Moss and blage was prominent in Budworth Mere, England Balls, 1989;Stoyneva,1994). The assemblage is (Reynolds, 1979b). sometimes more prominent in the plankton of The effects of nitrogen depletion in small, more substantial lakes, including Arresø, Den- shallow lakes are no different from other mark (Olrik, 1981), and during the more stable nutrient- and energy-rich habitats, where, of the alternating phases in the enriched Hamil- accordingly, nitrogen-fixing (H1) Anabaena and ton Harbour, Lake Ontario (Haffner et al., 1980). Anabaenopsis species and, inwarmlakes, (SN) At low latitudes, such enriched shallow sys- Cylindrospermopsis may be promoted. Both are tems may succumb to monospecific (or, at least, important components in Balaton, Europe’s monogeneric) steady-state blooms of Microcystis largest shallow lake (area 593 km2,meandepth (group M), where the alga’s ability to regulate 3.3 m: Padisak´ and Reynolds, 1998). The plank- its buoyancy helps it to avoid excessive light ton of humic-stained Fennoscandian lakes is near the surface during diurnal stability and frequently distinguished by the presence of chrys- to recover position after nocturnal mixing. The ophytes, cryptomonads and the raphidophyte original demonstration of dominance through Gonyostomum semen.Physiological studies on this this mechanism, by Ganf (1974b), in the tropi- alga by Korneva (2001)seemedtoReynoldset al. cal Lake George, Uganda (area 250 km2,mean (2002)tojustify its separation into group Q. The depth 2.5 m), has been repeated in subsequent plankton of acidic small shallow lakes is biased studies of other low-latitude, hypertrophic shal- towards chlorophyte (including desmid) and low lakes (Harding, 1997;Yuneset al., 1998). My chrysophyte genera. An interesting observation own, unpublished observations of the large but on the plankton of Oak Mere (area 0.2 km2,mean shallow lake Tai Hu (2425 km2,meandepth2.1 depth 2.1 m) was the replacement of a plank- m) suggest that Microcystis similarly dominates ton dominated successively by Ankistrodesmus, the plankton from quite early (April) in the year. SPECIES COMPOSITION AND TEMPORAL CHANGE 345

Finally, many shallow, hypertrophic lakes in low or is made shallow through density strati- the temperate regions (especially those exposed fication. Such benign conditions are presumed to frequent or continuous wind mixing), experi- to satisfy the minimum requirements of most ence year-round dominance by Planktothrix agard- phytoplankton. However, the most widely promi- hii and/or Limnothrix redekei or other slender, soli- nent trait-differentiated planktic groups achiev- tary filamentous Cyanobacteria, such as Pseudan- ing large, dominant and persistent populations abaena species. Phytoplankters of group S1 need under these conditions are epitomised by the never normally experience nutrient limitation, groups LM, M and R and, perhaps to a lesser and they are difficult for cladocerans to filter and extent, H1 and J (see also Naselli-Flores et al., for copepods to manipulate (although certain cil- 2003). iates seemtohaveperfectedameansofingesting Decreasing day length and/or deeper mix- them). They may dominate to the extent that they ing result in diminished opportunities for light- exclude almost all other autotrophic phytoplank- harvesting, to the extent that the capacity ton, to the limit of the energy-determined carry- forphotosynthetic fixation of inorganic carbon ing capacity set by their own highly efficient and becomes the constraint on the ability of phyto- persistent light-harvesting antennae (Reynolds, plankton to function and survive (as discussed 1994b). Several examples from the literature were in Section 5.4.3). It was argued there that the cited there in support, including the studies of more sensitive species are (literally) outcompeted Berger (1984, 1989,onthepolderlakes Dron- by those that are more robustly adaptable and termeer, Wolderwijd and the pre-manipulated predisposed to light interception and harvest. The Veluwemeer), of Whitton and Peat (1969,onSt survey in the present chapter would confirm that James’s Park, London) and of Gibson et al.(1971, late-summer mixing in temperate, mesotrophic on Lough Neagh, Northern Ireland). In Kasum- and eutrophic lakes repeatedly selects for P-group igaura (area 220 km2,meandepth4m),Plankto- diatoms and desmids, and in some instances, for thrix agardhii replaced Microcystis aeruginosa as one T-group Tribonema and Mougeotia and, especially, low-diversity plankton gave way to another (Taka- S1-group Planktothrix agardhii.Inhighly enriched, mura et al., 1992)and,apparently(Recknagel, shallow waters, dominance of self-shaded assem- 1997), as a consequence of an ongoing expansion blages by the latter may be near-perennial. Con- of the resource capacity demanding the better- versely, the biomass recruited during the ‘spring performing species under increasing light limi- outburst’ of phytoplankton in the mixed columns tation. of mesotrophic and mildly eutrophic temperate lakes is generally dominated by diatoms (B, C 7.2.4 Species assemblage patterns in lakes groups) and Y-group cryptomonads, gymnodini- Certain consistent patterns emerge from the ans or small peridinians. descriptive accounts making up Section 7.2.3, In many instances, improving light conditions most of which begin with a recognition that phy- in lakes press the constraints towards the nutri- toplankton production and the biomass that it is ent resources. Shortage of silicon is an obvious possible to support are often constrained by the selective disadvantage to all diatom groups but environmental conditions obtaining. A corollary it is not clear from the present review that sili- to this statement is that high rates of produc- con deficiency becomes a limiting factor among tion, sustaining and maintaining large planktic themost oligotrophic lakes (that is, other nutri- crops, depend upon the alleviation of the typ- ents intervene first). The instances in which nitro- ical constraining factors. Standing-crop concen- gen, theoretically or by interpretation, seems to trations in excess of 40 µgchla L−1 are mainly limit the supportive capacity are more common encountered in lowland and moraine lakes. All than the weight of literature might suggest, espe- of these offer a substantial base of bioavail- cially at low latitudes and in well-leached catch- able nutrients, especially phosphorus and nitro- ments. Nitrogen deficiency may be cited as a gen. Moreover, autotrophs benefit from being selective factor operating in favour of the com- entrained within a layer that is absolutely shal- mon occurrence of H1, H2 and, in warm-water 346 COMMUNITY ASSEMBLY IN THE PLANKTON

locations, SN groups of nitrogen-fixers. However, among smaller lakes that stratify to within 10 it must be emphasised again that their preva- mofthe water surface and where accessible lence is not confined to habitats that are low SRP concentrations persist in the metalimnion, in nitrate or ammonium. Moreover, the argued themost successful species are the relatively dependence of the ability to fix nitrogen on high motile gleaner species (of especially groups LO energy inputs and an adequate reserve of phos- and LM). Given water of sufficient clarity these phorus and trace metals (see Section 4.4.3)issup- may well be able to operate successfully simply ported by the survey (see, especially, p. 335). In by remaining at depth. However, the deeper are stratified lakes, conditions of low DIN and low the available resources, the more important is SRP may be more amenable to motile ‘gleaners’, thelight-harvesting ability and the less impor- including those with known phagotrophic capa- tant is rapid motility. Ultimately, before energy bilities. This explanation fits the frequent domi- and nutrient resources are finally uncoupled, the nance of E, U and, especially, LO groups of algae. selective advantage may fall to superior, chro- In water columns that are chronically deficient in matically adapted light-harvesting species with nitrogen and phosphorus and, thus, in the ability asimultaneous ability to maintain and adjust to develop even a detrital store of nutrients, the vertical station – and include cryptomonads (Y) most tolerant survivors appear to be the Z-group and phycoerythin-rich Cyanobacteria, especially picocyanobacteria. Planktothrix rubescens (R). Phosphorus bioavailability, however, remains The surveyed cases support the contention amajorconstraintuponthe supportive capacity that particular adaptive traits distinguished in a large number of stratifying and shallow lakes among the phytoplankton and the species in and, hence, a key factor in defining the trophic which they are most strongly represented are state. It has been recognised in earlier chapters better suited to particular sets of environmental that plankton algae are generally very effective conditions. The more severe are the latter, the in garnering their own phosphorus requirements greater the selective power that works in favour from SRP concentrations as low as 10−7 M(∼3 of the most tolerant species. This is the comple- µgPL−1)(seep.158). While greater concentra- mentary deduction to that of Dufrêne and Leg- tions than this remain accessible, the supportive endre (1997)regarding the reliability of indica- capacity of BAP has not been reached. Superior torspecies and what they may convey in terms affinity for phosphorus in solution is unlikely of constraints acting upon community function. to confer a competitive advantage to phytoplank- There is an obvious mutualism between, on the ton exceptintherange10−9–10−7 M. In those one hand, evolutionary strategies and adapta- instances where BAP is always ornearlyalways tions of species that permit them to tolerate <10−7 M(∼3 µgPL−1), species with high uptake particular environmental conditions and, on the affinities experience both the immediate com- other, the conspicuous occurrence of these same petitive advantage of winning resources and the species in locations where the critical conditions longer-term advantage from being able to main- obtain. InTable7.6,the various trait-separated tain larger inocula from one growth opportu- functional groups are listed in terms of their nity to the next (seep.203). The trait is shared reactivity to selective variables distinguishing among species identified in Table 5.2 and which among habitats or, for a given habitat, among figure in groups A, E, F, N, U, X3 and Z. They seasonally varying conditions. are represented in lakes throughout the descrip- Of course, alternative approaches are avail- tive series but they provide the prominent com- able to establishing the link between organismic ponents of the planktic assemblages in the low- adaptations and indicative habitat preferences. Poligotrophic lakes, large and small. They are Forinstance, it is commonly revealed through also well represented among those stratifying analysis of the size distributions of the total- mesotrophic waters during periods in which epil- ity of organisms forming the assemblage, inde- imnetic BAP has been previously be depleted pendently of its taxonomic composition, based to levels of ≥10−8 M(∼0.3 µgPL−1). However, instead upon their functional contributions SPECIES COMPOSITION AND TEMPORAL CHANGE 347

Ta b l e 7.6 Sensitivities to habitat properties of functional groups of phytoplankton

∗ hm I θ [P] [N] [Si] [CO2] f Group <3 <1.5 <8 <10−7 <10−6 <10−5 <10−5 <0.4 A − ? ++++−− B −+++−−−− C −++−−−? − D +++−−−+− N −−−+−+/−− ? P −−−−−+/−+ + T − ? −+/−− + ? + S1 +++−−+++ S2 + +−−−+++ SN ++−−++++ Z +−++++? − X3 +−++−+−− X2 + − + ? − + ? − X1 + − + −−++− Y +++−−+ ? − E ++++− + −− F + − ++− + −− G + − + −−+++ J + ? + −−+ ? − K + ? −−−++? H1, H2 + −−−++++ U + − ? + − + − + LO + −−+ − + − + LM + −−−−+++ M + −−−−−++ R +++−−+ ? + V +++−−+ ? − W1 +++−−+ ? − W2 ? Q +++??+ −−

Notes: Entries in table are to denote tolerance (+)ornopositive beneﬁt (−)ofthe environmental condition set; ‘+/−’isused to denote that some species in the association are tolerant; ‘?’ denotes that tolerance suspected but not proven. Some representative genera or species only are listed. Variables signiﬁed are: depth of surface mixed layer (hm,inmfrom surface); mean daily irradiance levels experienced (I∗,inmol photons m−2 d−1); water temperature (θ,in◦C); the concentration of soluble reactive phosphorus ([P], in mol L−1); the concentration of dissolved inorganic nitrogen ([N], in mol L−1); the concentration of soluble reactive silicon ([Si], in mol L−1); the concentration of dissolved −1 carbon dioxide ([CO2], in mol L ); and the proportion of the water processed each day by rotiferan and crustacean zooplankton (f ) Source: Updated from Reynolds (2000a). 348 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.7 Schematic summary of freshwater pelagic habitats, deﬁned in terms of I∗∗ (an integral of light income and its dilution through the mixed layer) and K∗∗ (an integral of nutrient accessibility), and where ∗∗ 1/2 −1 ∗∗ I = (I 0·Im) hm and K = [K]/(1 + δ[K]); for further details see text. Redrawn with permission from Reynolds (1999a).

(Bailey-Watts, 1978;Gaedke and Straile, 1994b). this applies to photoautotrophic picoplankton as Size-spectral analyses are particularly sensitive to much as to nanoplankton (Carrick and Schelske, thestructure of the pelagic food web and its 1997). High concentrations of picophytoplank- responses to interannual enviromental variabil- ton dominated the algal assemblage of a small ity and to fundamental alterations to the nutri- Antarctic pond, under the conditions of low ent base(Gaedke,1998). However, care is needed ambient temperatures and nutrient enrichment in making ecological interpretations from algal through its use as a roost by elephant seals (Iza- morphometry without allowing for its alterna- guirre et al., 2001). tive indications. For instance, the many sepa- The truth is that smaller algae have physiolog- rate studies on the abundance and production of ical and dynamic advantages over large ones. It is picophytoplankton support the conclusion that theintervention of other factors (most especially, these organisms fulfil the major contribution to the influence of grazing and the segregation of the carbon dynamics of oligotrophic pelagic sys- theenergy and resource bases) that alters the tems (Stockner and Antia, 1986;Chisholm et al., structural balance in favour of larger or motile 1988;Agawin et al., 2000;Pick,2000). In contrast, algae. This too impinges upon the spectral anal- the greatest concentrations of large algae like ysis. In reality, the procedure detects functional Ceratium and Microcystis are supposedly excluded aspects of the assemblage and the extent of its from nutrient-poor systems (Wolf-Gladrow and successional maturity with respect to the driving Riebesell, 1997). Thus, a size spectrum biassed variables and not necessarily what the limiting towards a predominance of smaller or larger variables might be. formsshould reflect a lesser or greater produc- To summarise the compositional patterns of tive capacity. The counter to this simplicity is freshwater phytoplankton assemblages, a habi- that, indeed, organisms at the diminutive end tat template, analogous to the one for marine of the size spectrum gain full advantage of their environments (Fig. 7.4), is proposed in Fig. 7.7. high surface-to-volume ratio to acquire and con- Habitats are characterised on axes of nutrient vert resources into biomass faster than larger resources and energy distribution, the interac- organisms with less favourable surface-to-volume tion of which is suggested to drive the pri- ratio lowers(Raven,1998)(see also Section 5.3.1). mary selective criteria in lakes (variations in Other things being equal, then, the greater is acidity/alkalinity are not addressed specifically). theproductive capacity, the more the size spec- Unlike Fig. 7.4,however,theaxes are quanti- trum should be biassed towards smaller rather fied, following Reynolds (1999a), in units that than larger forms. Recent research confirms that were designed to embrace variabilities in both SPECIES COMPOSITION AND TEMPORAL CHANGE 349

−3 −1 Figure 7.8 (a) Habitat template for trait-separated photons m d .Using actual measurements categories of freshwater phytoplankton (cf. Table 7.1), based (Ganf, 1974b)ofaveragedailyirradiance at on limitation gradients of decreasing energy harvest and equatorial Lake George (average daily irradiance accessible resources, as originally envisaged by Reynolds ∼2000 J cm−2 d−1,or20MJm−2 d−1,PAR∼9.4 (1987b). The superimposition of one shape on another MJ m−2 d−1 = 43 mol photon m−2 d−1) and verti- implies that the algal category is more likely to succeed than cal extinction coefficients through a 2.5-m water those that it obscures. (b) As (a) but unlabelled; the shaded column of up to 7.7 m−1, I∗∗ falls as low as 1.45 triangles embrace approximately the floristic representation −3 −1 in the named systems: 1, eutrophic pools in Shropshire; 2, mmol photons m d Similarly, at the end of Montezuma’s Well; 3, polder lakes such as Veluwemeer; 4, thesummer in the Araucanian lake Nauel Huapi Norfolk Broads; 5, Hamilton Harbour, Lake Ontario; 6, Crose (p. 336), even a low attenuation coefficient (ελ ≤ − Mere; 7, Lough Neagh; 8, Volta Grande Reservoir; 9, Lagoa 0.2 m 1) does not prevent convectional mixing Carioca; 10, Windermere, pre-1965; 11, Millstättersee. to 60 m from diluting the light availability to a Redrawn with permission from Reynolds (1997a). similar level (I∗∗ ∼1.2 mmol photons m−3 d−1). The vertical scale (K∗∗)isbased upon mixed- deep and shallow lakes. The scale of the hori- ∗∗ layer nutrient concentration, divided by a factor zontal axis, I ,integrates the income of photo- based on the concentration gradient (1 + δ[K]) synthetic energy not just through time but its ∗ through the whole trophogenic layer. This index dilution through the mixed layer. Whereas I , distinguishes chronic deficiency of the critical from Eq. (3.17), is calculated from the average nutrient ([K]low,δ[K]low,soK∗∗ = [K]/(1 + δ[K]) is vertical absorptance of photosynthetically active also low) from the effects of near-surface deple- ∗ = ∗∗ solar radiation over the mixed depth (hm)[asI tion (as δ[K]increases, so K decreases. In terms · 1/2 = · −ε (I 0 Im) , where Im I 0 hm exp( λ)isthe of phosphorus, for example, the review lakes residual irradiance flux reaching the base of the ∗∗ cover a range of measured availabilities from 0.01 mixed layer], I is the average harvestable photon to 25 µM (0.3 to 750 µgPL−1). However, the scale concentration. responds to the seasonal depletion of resources Thus, in the surface mixed layer to the point of critical 1 ∗∗ /2 −1 deficiency. I = (I · Im) h (7.1) 0 m Earlier versions of this template (especially in If daily integrals of the photon flux are used, Reynolds 1987b, c;seealsooverview in Reynolds, we can distinguish not just high from low light 2003a)havebeen used to accommodate the distri- incomes but compare dilution of the income as a butions of most of the trait-separated functional consequence of mixed layer depth and turbidity. groups. The shapes drawn in Fig. 7.8aarepro- For example,aphoton flux of 60 mol photons posed to represent the respective environmental −2 −1 m d on a shallow water body (hm = H = 1 limits of each of the algal groups, with group-S m) with a low coefficient of vertical light extinc- species extending furthest rightwards along the − ∗∗ ∗∗ tion (say ελ = 0.2 m 1), I solves at 54.3 mol I scale (shallow hypertrophic habitatats) and 350 COMMUNITY ASSEMBLY IN THE PLANKTON

the general track shown in Fig. 7.9. This pur- ports to move through summer stratiﬁcation, nutrient depletion, autumnal mixing (less light, re-enrichment and nutrient uptake during the spring mixing). In theory, at least, the trajectory inserted into each of the triangles superimposed onto Fig. 7.8bshould be capable of describing the compositional changes that characterise the annual plankton cycles in the water bodies represented. At least the pattern, if not the detail, of phytoplankton structure is captured.

Figure 7.9 Idealised year-long timetrack of the selectivity 7.3 Assembly processes in the trajectory imposed by seasonal variability in a temperate system, in relation to the zones favoured by C, S and R phytoplankton primary strategists. Redrawn with permission from Smayda and Reynolds (2001). The purpose of the present section is to explore the active mechanisms that influence the vari- group-E dinoflagellates furthest downwards in ations in the structure of the phytoplankton the K∗∗ axis (depleting epilimnia of oligotrophic in natural communities, according to circum- lakes). Less tolerant groups terminate closer to stances and dominant functional constraints. the origin intheupper left-hand corner repre- The objective is to determine the extent of presenting resource-rich, energy-rich habitats. Super- dictability of natural communities, with the imposition of shapes, one upon another, implies processes quantified wherever possible. The key superior group performances, with the fastest topics considered to be relevant to community nutrient- and light-saturated growth rates of X1 assembly in the plankton – species richness and species dominating the top left-hand corner. diversity, trait selection, succession and stabil- This representation is illustrative but it helps ity, structural disturbance and organisational to put into perspective the floristic descriptions resilience – are no different from those believed of many kinds of lakes on to a single two- to impinge upon the community ecology of other dimensional figure. The representation in Fig systems. However, the dynamics of pelagic sys- 7.8bisidentical to that in Fig. 7.8a, but for the tems operate at such absolutely small timescales stripping out of all the alphanumeric insertions. (when compared with those of terrestrial sys- The numbered triangles that replace them are tems) that the outcomes are not only observable really quite effective in circumscribing the plank- phenomena, as opposed to speculative extrapola- tic flora of named lakes or lake series. These tions, but they are amenable to meaningful, con- include shallow, enriched pools and well-flushed trolled experimental manipulation. This is the pools (1, 2), the turbid, Plankothrix-dominated part of the book in which the community ecology polder lakes (3), through to oligotrophic lakes of the phytoplankton can be championed as the such as Millstattersee¨ (11). model for community ecological processes every- Collectively, the shapes used in Fig. 7.8 com- where. Some of the terms used require clarifica- prise the familiar triangular layout, correspond- tion of usage; some working definitions are given ing to the disposition of the primary algal in Box 7.1. strategies (with C, R and S at the apices). Sea- sonal changes in any individual system will, to 7.3.1 Assembly of nascent communities agreater or lesser extent, be tracked through The first challenge of this discussion is to estab- the triangle, in terms of variations in I∗∗ and lish whether the observable assemblages of dif- imposed changes in resource accessibility, along ferent species of phytoplankton (and, for that ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 351 matter, cohabitant microbes, zooplankton and waythat material cycling is internalised and, to nekton) are merely fortuitous and random com- alargeextent, closed’ (Ripl and Wolter, 2003,p. binations of species that happen to be present, 300). The components are: by chance and in sufficient concentrations to be (1) Primary producers, which manufacture encountered readily, or whether these are selec- organic material and supply the energy tively biassed, invoking either mutually interspe- needed for all heterotrophic structures. cific dependence or mutual tolerance. If the lat- (2) Water, as a moderating feedback control of ter, then the central question becomes ‘How are production. they put together?’ (3) Areservoir of organic detritus. (4) Decomposers – bacteria and fungi – draw- Minimal communities ing energy from the oxidation of detrital The word ‘community’ presupposes some sort stores, which process also recycles nutrients of functional differentiation, with populations and minerals to primary producers; the store of several species each doing different things is exploited efficiently and with a low level but whose activities, in total, achieve some of losses. linked reactivity that defines their combined out- (5) The food web – that network of consumers puts – the community function. Historically, ecol- comprising higher and lower animals ogists have experienced difficulties in defining through whose activities much of the thenature of communities. At one extreme, original energetic input is finally dissipated. Clements (1916)anticipated a supra-organismic regulation of tightly bound organismic func- It need hardly be added that the remarks of Ripl tions. At the other, Gleason (1917, 1927) coun- and Wolter (2003)wereinspired by a view of ter- tered that the species were present more or less restrial ecosystems. Yet, but for an alternative by chance. Thus, species composition is funda- emphasis on the relevance of water and a ten- mentally non-predictable beyond the influence of dency of open waters to store organic detritus species-specific habitat preferences and the con- remotely (i.e. in the sediments), the model ade- sequence of selective interspecific interactions, quately describes a self-sufficient pelagic ecosys- including predation and competition. Current tem. Moreover, in either case, although all the thinking is rather closer to the second view than biotic components are essential to the sustain- thefirst but the interactions are recognised to able, integrated function of the whole structure, be crucial and far from straightforward. A help- primary producers play a critical role in inter- ful modern model is that of Ripl and Wolter ceding in the dissipative flux, in synthesising the (2003), which envisages community function as organic base and, hence, in initiating the assem- aseries of successive organisational hierarchies, bly of the ecological unit. This will be taken as beginning with the interdependence of molec- asufficient justification for concentrating upon ular transformations and working through to assembly processes among aquatic primary pro- thephysiological control of individual organisms ducers (and, especially, the phytoplankton) and and to the beneficial coordination of the separate for deferring consideration of the assembly of the activities of the various component organisms. heterotrophic and phagotrophic elements of the They cited several illustrative examples, includ- pelagic community to Section 7.3.2. ing the nitrogen-fixing symbionts of water plants Of special interest are the answers to the (including diatoms) and the use of algal exudates questions, how many and which species of pri- by bacteria. They proposed the DEU (for dissipa- mary producer will be present? The supposition tive ecological unit) as the minimal interspeci- made throughout this book is that phytoplank- fic assembly within which entities contribute tonspecies will grow wherever and whenever to an organised, functioning structure with a they can, provided that (i) the supportive capac- measurable and increasing thermodynamic effi- ity to satisfy their minimal requirements for ciency. Thus, the DEU comprises five distinct com- their growth is in place and (ii), coincidentally, ponents, capable of mutual coupling ‘in such a viable propagules are already present and able to 352 COMMUNITY ASSEMBLY IN THE PLANKTON

take advantage of the amenable conditions. Ear- upstream location (including the river itself) is lier chapters have probed extensively the inter- likely to deliver an inoculum of phytoplankton specific differences in environmental require- with a composition reflecting the upstream habi- ments and tolerances but the uncertainties relat- tats that supplied it. Species that produce ben- ing to propagule dispersion have, so far, been thic resting spores and propagules and which avoided. were previously resident in the plankton of the Both issues are relevant to the role of species flushed lake and which succeeded in recruit- richness and diversity in assembling communi- ing a large number of overwintering propag- ties. It has to be admitted, however, that the ules to the sediment prior to displacement of large numbers of widely distributed species with thewater mass by throughflow will also enjoy generally rather small differences in their basic abiassed opportunity to recruit inocula to the requirements do not offer clear prospects for expanding development opportunity. In spite of separating critical processes. Thus, it helpful to this, the number of species colonising and, cer- consider the governing principles as they are tainly, the relative numbers of individual organ- expressed in the establishment phases of new, isms of each contributed is mainly a matter of open and pristine habitats. This approach fol- chance (Talling, 1951). The larger the system and lows the powerful ‘island biogeographic’ concept, thegreater its spatio-temporal connectivities, the developed by MacArthur and Wilson (1967)to greater is the likelihood of annually reproducible describe the processes leading to the establish- patterns. ment of a biotic ecosystem onanewlyformed In large and small systems alike, however, island, arising Surtsey-like from the ocean. The the one statement that seems true is that the model translates well to the context of phyto- species that initially become abundant either plankton development in a small, temperate or ‘arrive’ (with or without the benefit of a rest- sub-polar, inland water body, which, in this case, ing inoculum) in strength, or grow rapidly, may be considered as an aquatic island in a ter- or they do both. These traits are analogous restrial sea. Seasonality confers an element of to those of the pioneering, invasive, island- vernal ‘newness’ of such a habitat. If objection colonising species of MacArthur and Wilson be made to the bias attributable to the pres- (1967), (r-)selected by their investment in short ence of overwintering of propagules, then the life histories and prolific production of small, eas- case of flood-plain lakes (varzeas) left isolated ily transmissible seeds. The corresponding phyto- by falling rivers (Garc´ıa de Emiliani, 1993)or plankters are manifestly the small-celled, quick- of mining subsidence pools (e.g. Dumont, 1999) growing C-strategist species (Section 5.4.5)(Box could be adopted. In the open sea, the seasonal 5.1). Freshwater examples come from the X1, X2 onset of thermal stratification in a water column and Y functional groups (Section 7.2.3;Table 7.1). ‘sterilised’ of phytoplankton during months of Indeed, some of the species involved (of such gen- deep mixing also conveys the idea of open, avail- era as Chlorella, Chlamydomonas, Chlorococcum, Cocco- able habitat, depauperate in indigenous plank- myxa, Diacanthos, Golenkinia, Micractinium, Mono- tic algae. Even highly flushed, river-fed small raphidium, Treubaria, Westella)are also variously lakes (like Grasmere, English Lake District), may encountered in small or temporary aquatic habi- become so depleted of phytoplankton during wet tats, such as rain puddles of a few days’ age, periods that, effectively, they become amenable, bird baths, rinsing water left in open contain- open habitat for the next phytoplankters to arrive ers and bottles, and in the phytotelmatic habi- there (Reynolds and Lund, 1988). tats of water retained in the foliage of epiphytic plants such as bromeliads. The only consistently The pioneer element of nascent communities plausible means of dispersal for propagules of In the truly novel planktic habitat, the first these algae is through the air. The extent of colonists have to arrive, de novo,fromsome spore production and the tolerance of dessica- other external location. In other, quasi-open habi- tion is not well known, while the viability of tats, fluvial transport of propagules from an cells in aerosols needs further investigation. The ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 353 point that needs to be emphasised is that small, Each was previously unrecorded in the lake and, potentially planktic, C-strategist algae are not supposedly, recruited from the nearest sea, some just highly mobile between mutually isolated, 1500 km distant! potentially viable habitats but that, collectively, The implication of this ready colonisation they are sufficiently abundant to have an evi- by invasive species is that, for some species at dently high probability of early colonisation of least, the dispersal channels are effective and new planktic habitats. well exploited. Not all species are equally mobile: The observation is relevant to one of those colonial Cyanobacteria such as Microcystis are rel- enduring puzzles of phytoplankton ecology, still atively slow to establish in newly enriched lakes, lacking formal solution, which is just how appar- even though the habitat might seems amenable ently conspecific phytoplankters move among to its growth (Sas, 1989). A number of species have hydrologically isolated lakes and achieve near- very limited distributions and seem endemic to global, cosmopolitan distributions. Many con- particular regions or even localities (Tyler, 1996). tributory investigations, for instance, those of However, water bodies throughout most of the Maguire (1963), Atkinson (1980)andKristiansen world, not just new ones, must be constantly (1996), reveal something of the variety and vari- assailed by the propagules of invasive species. ability of dispersal routes for planktic organisms, This process helps to maintain their apparent especially aquatic insects and water birds. Rather cosmopolitan and pandemic distributions. These less than the much-speculated ‘duck’s foot’, guts species turn up everywhere and, if the opportu- and faeces and avian feathers retain propagules nity of habitat suitability and resource availabil- and (often) live vegetative algal cells, providing ity is there, populations may establish wherever important avenues for the potential transfer of they land. planktic inocula from one water body to another. These deductions apply to many bacteria and This may apply over relatively modest distances, other microorganisms and, to a lesser extent, to before desiccation or digestion destroys the via- mesozooplankters (Dumont, 1999). They apply at bility of the potential inocula. Recent investiga- an approximately comparable level among the tions by Okamura and her co-workers (see espe- microzooplanktic and nanozooplanktic ciliates, cially Bilton et al., 2001;Freeland et al., 2001) studied extensively by Finlay (2002). Besides coin- have related the spread of genetically separa- ciding with the size ranges and body masses ble clones of sessile bryozoans (small aquatic of dispersive phytoplankton, ciliates also occur filter-feeders that produce distinctive propagules locally in abundance and enjoy world-wide ubiq- called statoblasts) to the migratory paths of wild- uity, and, as Finlay’s experiments amply demon- fowl. The work makes it clear that avian move- strate, common ecotypic species quickly estab- ments do greatly influence the genomic compo- lish in contrived new environments open to their sition and species richness of island freshwater colonisation from the atmosphere. Ubiquity is communities. dependent upon mobility of propagules, which Even marine phytoplankton is readily trans- is, in turn, a function of propagule size. Then portable via other agents. The recent diminution their relative transmissibilities are subject to the in the area and standing volume of the Aralskoye influence of distance and physical barriers. Moun- More, as a result of disastrous mismanagement of tain ranges and oceans may constrain the dis- its hydrology over the past few decades (see e.g. tributions of aquatic invertebrates and insects. Aladin et al., 1993) has been accompanied by a Fish experience similar difficulties, even on a rise in its salinity. In the 1990s, by the time that catchment-to-catchment basis. Aquatic mammals thesalinity had reached 28–30 mg L−1,productiv- spread to places that they can walk or swim to. ity had collapsed and all freshwater and brackish Finlay’s (2002)hypothetical separation of protist species of phytoplankton had been eliminated. species that are ubiquists from those that have According to Koroleva (1993), the depleted plank- biogeographies on the basis of their sizes (criti- tic flora included marine species of Exuviella, Pro- cal range, ∼1mm) appears to hold for all pelagic rocentrum, Actinocyclus, Chaetoceros and Cyclotella. organisms. 354 COMMUNITY ASSEMBLY IN THE PLANKTON

Species richness of nascent communities number of niches is a reasonable assumption. Planktic colonisation of new habitat or the Fitted to species lists of macroscopic flora and reopening of existing habitat through the sea- fauna of existing islands, Eq. (7.3) has been found sonal relaxation of physical exclusions may be to account for up to 70% of the variability in expressed in quantitative terms as the filling of species number. The slope, z,isreciprocal to previously unoccupied niches, or the opportuni- theimmigration rates and, in these cases, usu- ties available for the exploitation of the aggre- ally solves at between 0.2 and 0.35. Similar val- gate pool of resources. The more that the niches ues have been obtained when the solution has become occupied, the slower is the process of been applied to the occurrences of phytophagous filling. MacArthur and Wilson (1967)formulated insects on their food-plant ‘islands’, though val- adifferential equation (7.2)todescribecolonisa- ues are conspicuously influenced by the abun- tion, thus: dance (thus mutual proximity and accessibility) of hosts (Janzen, 1968;LawtonandSchroder,¨ / / = − 1 n(t)dn dt uˆ(ñ n)(7.2) 1977). Smaller values of z (0.1–0.2) represent where n(t)isthenumber of exploitable niches in enhanced opportunities for immigration. Inter- thelocation at a time t, ñ is the number reached phyletic differences in immigration rates to given at t =∞and uˆ is the rate at which they are filled. locations are also apparent. For instance, birds Practical solution of the equation is not possi- have lower z values than land snails. Finlay et al. ble without independent quantification of the (1998)haveworked out that the slope z forfresh- number of potential niches (ñ)andexperimental waterplanktic ciliates is yet smaller again (z = observations on the arrival of occupant species 0.043) as a consequence of their rapid rates of (uˆ). Occupancy is asymptotic to ñ but its value is dispersal. difficult to predict from observation, especially Ifalowvalueofz in Eq. (7.3)reciprocates in the early stages of colonisation, when the ahigh initial dispersive value of uˆ in Eq. (7.2), resource availability (S)islikelytobelargeinrela- thepotential richness of planktic species may tion to the exploitative demand (D). Thus, what approach the maximum (ñ)that the habitat- may be, effectively, a single broad niche may be size constraint will allow. Certainly, in those simultaneously and non-competitively exploited instances where investigations of species struc- by several species, which together act as a multi- ture has been sufficiently competent and exhaus- species guild, or functional group, of species tive, the species richness of individual lake sys- (Tokeshi, 1997). However, it is readily predictable tems is demonstrably large. Dumont and Segers that the number of distingushable and viable (1996)estimated the likely maximum species niches is likely to be a function of the size of the richness of cladocerans to be ∼50 and of rotifers habitat (a large lake offers more colonist oppor- to be ≤270. Representation by a significant pro- tunities than, say, a pool in a bromeliad). This portion of the extrapolated global total of ∼3000 is back-extrapolable from another prediction of species of free-living ciliates is probable (Finlay et island biogeography, pointed out by MacArthur al., 1998). Compared to a supposed potential of and Wilson (1967)andsupported empirically in 4000 to 5000 taxa, 435 named species of fresh- several subsequent investigations, that there will waterphytoplankton in tropical Lake Lanao were be a positive correlation between the species rich- noted by Lewis (1978). Consecutive daily sam- ness of an island and its size. The number of ples of the phytoplankton of shallow Lake Bal- species (n )tobefoundinadefinedarea,A, con- sp aton accumulated a list of 417 separate taxa forms totherelationship in 211 days (only ∼300 were considered to be z truly planktic: Padisak,´ 1992). The accumulated nsp = k A (7.3) species list of phytoplankton encountered in Win- where k and z are characteristics of particular dermere (Reynolds and Irish, 2000)includes 146 categories of organisms and invasiveness. The named taxa. In samples of phytoplankton from existence of at least an approximately equivalent the upper 100 m of the central North Pacific ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 355 overa12-year period, Venrick (1990)recorded 245 organic carbon, which is powered ultimately by species. short-wavelength, photosynthetically active solar energy. The role of the phototrophic primary pro- 7.3.2 Properties of accumulating ducers is to intercept, harvest and invest energy communities in the production of high-energy organic carbon Following the establishment (or re-establishment) compounds. This process is continuously subject of an assemblage of colonist primary producers, to the lawsofthermodynamics. The second of many subsequent events are set in train. Fur- these determines that the direction of flow is ther species of primary producers may arrive and from the concentrated to the diffuse and that respond positively to the favourable growth con- short-wavelength energy is dispersed irrecover- ditions. Total biomass increases and individuals ably at longer wavelengths (i.e. as heat). Short- begin to impinge on each other’s environments, wave electromagnetic solar radiation falling on inevitably setting up interspecific interactions. alifeless planet causes molecular excitation and Moreover, the accumulation of producer biomass, dispersion (a rise in the surface temperature) but detritus and organic waste soon constitutes food most is back-reflected to space at longer wave- and substrate for the heterotrophs (phagotrophic lengths. This dissipation of heat is irreversible. herbivores, microbial decomposers) and the open- It follows that the effectofapulseofenergyis ing of primary product as a resource to consumer to reduce order and increase randomness, or, in components of the DEU (Ripl and Wolter, 2002); thermodynamic terms, to raise the entropy of the the functional community is born! recipient structures. Several aspects of this development command Against the inevitability of entropic dissi- our attention. Intercepting an increasing por- pation, the ability of growing communities to tion of the solar flux, the accumulating sys- assemble structure, order and complexity seems, tem involvesthedeployment of greater levels at first sight, to be in contravention of the laws of power and resources. Sooner or later, con- of the universe (Prigogine, 1955). In truth, ecosys- straints in the supply of one or the other feed tems are an integral part of the thermodynamic back, invoking adaptive reactions in the pat- system, doing little more than to reroute and reg- tern of community assembly. In turn, there ulate the velocity of the dissipative flux. A reason- are consequences for species composition, rich- able analogy is that of a waterwheel located on ness, dominance and diversity, and key species astream (Reynolds, 2001a). Some of the kinetic thus favoured characterise the overall commu- energy of flow is drawn to drive the wheel nity function. These developments are some- (the energy-harvesting primary producers), whose times referred to collectively as community ‘self- motion may be exploited as a source of alterna- organisation’ (or autopoesis:see, for instance, Pahl- tive mechanical or electrical power (the ecosys- Wostl, 1995). They are, indeed, contingent upon tem). However, the overall direction of the flow is behaviours and mutual interactions at the basic unaltered. levels of community assembly (the predilections Moreover, the proportion of the available and adaptabilities of the individual participating power that is realised in assembled biomass is species) and the aggregate of which is the struc- really quite small. Chlorophyll harvests no more ture and future of the emerging community. The than ∼6% of the radiative flux to which it is process of increasing system throughput, infor- exposed (at sub-saturating levels); barely 1.5–2% mation and complexity of network flows is also of the available energy is captured in carbon fix- known as ascendency (Ulanowicz, 1986)(seealso ation (Section 3.5.3). Much the largest propor- Box 7.1). tion (≤95%) of the solar flux is consumed in non-biological (but often biologically important) Ascendency: power and exergy processes, such as heating the water and driv- These concepts are not difficult to grasp if the ing evaporation and cooling. The investment of appropriate analogies are used. Biological sys- thephotosynthetically active radiation actually tems are organised about the managed flow of absorbed into plant biomass, typically ≥0.08 mol 356 COMMUNITY ASSEMBLY IN THE PLANKTON

the community, the DEU or the ecosystem, these Figure 7.10 Ecosystems and the dissipative energy flux. In structures dissipate energy, just as surely as the an abiotic world (a) all the incoming short-wave radiation, Qs, is reflected or reradiated at longer wavelengths (i.e. as heat). abiotic environment, and, ultimately, they do so This entropic disssipation is noted as dS and, in (a), is external to the point of balanced exchanges. to living organisms (hence dSe). The intervention of The apparent affront to the second thermody- photoautotrophic organisms intercepts and reroutes a namic law is that the inward flux may not be dis- fraction of the solar flux to drive the assembly of biogenic sipated at once but, instead, be retained within material. Much of this eventually shed in respiration and molecular bonds. While these persist, they block decomposition (as dSi), in conformity with thermodynamic entropy. In effect, the biological system is siphon- law, but only after the captured energy has been invested in ing off a part of the energy flux into a loop of the assembly and accumulation of biomass. This flux is equivalent to system exergy. A positive exergy flux enables reduced carbon, whence its eventual release is ecosystems to build, perhaps to the point where all the entire regulated and delayed. This entropy-free poten- solar flux is dissipated as dSi. B, biomass. Redrawn with tial has been variously referred to as negen- permission from Reynolds (1997a). tropy (for negative entropy) or exergy (Mejer and Jørgensen, 1979). Equally, it has been conceptu- − − C(molphoton) 1,or0.2 MJ (g C) 1,againat alised in different ways, in terms of informa- sub-saturating fluxes (Section 3.2.3), implies that tion stored (Salomonsen, 1992)orthesize of the thepower requirement to assemble producer accumulated gene pool (Jørgensen et al., 1995; − biomass is around 20 MJ (g C) 1. There is a further Jørgensen, 1999). energetic cost to assembling and maintaining Here, the preference is to adhere to expres- thestructure, which is met from the controlled sion in units of energetic fluxes (cf. Nielsen, 1992). metabolic re-oxidation (R)ofpart of the accumu- Then, one of the preconditions for community lated carbon. When producer biomass becomes ascendency is that the rate of energy harvest- part of the biomass of its consumer, some 40–90% ing and deployment in organic carbon synthe- of the power investment may be dissipated as sis shall exceed the aggregate of the require- heat. This is repeated at each successive trophic ment of internal maintenance and its dissipa- level. Alternatively, the cadavers and waste prod- tive losses. The cartoon in Fig. 7.10 illustrates the ucts may be exploited by decomposers for the increasing biomass of an ascendent community last molecules of organic carbon and the last ves- through time, from bare ground to high forest. tiges of the power investment. Whether we take From wholly dissipating the flux of short-wave ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 357

−2 −2 radiation (Qs)asheat(units,Wm or J m d−1), the intervention of biological systems is to reroute part of the dissipative flux (dS)intothe building (P)andmaintenance (R)ofbiomass (B). That part of the abiotic flux that is now passed through organisms is now distinguished as (dSi), leaving a reduced portion (dSe)ofthe original abiotic flux external to the organisms. For B to accumulate, the sum (dSi) + (dSe)hastobesmaller than the original flux, dS.Asbiomass is accumulated, R increases absolutely. Although more energy is siphoned off, absolutely more (and, eventually a bigger proportion) is dissipated as heat (dSi). The achievable steady state is when the biotic component harvests the entire energy flux (dSe → 0) and consumes it exclusively in its own maintenance (R = dSi → dS). No further increase is then possible: the community has achieved its highest state (Fig. 7.10c). Data are not available to quantify all the rele- Figure 7.11 Graphical representation, based on Fig. 3.18, of the relationships sketched in Fig. 7.10. The vertical axis vant fluxes. However, the principles can be illus- represents the incoming short-wave radiation. The curve trated by adopting the light-harvesting proper- represents the proportion that is ‘siphoned off’ into primary ties and phototrophic growth of the alga Chlorella production, thereby (temporarily) reducing the external (from Fig. 3.18)toscale the theoretical ability dissipative flux (hence, –dSe). The efficiency reduces with (and diminishing efficiency) of the producers to increasing mutual interference of the producer harvest and allocate the maximum energetic flux. light-harvesting but whose the maintenance costs (dSi)are The revised plot, in Fig. 7.11,showshow low, supposed to be proportional to the biomass. The energy − + pioneer levels of biomass harvest more energy difference between the curves ( dSe dSi)isavailable to than they expend and that the resultant posi- support growth, reproduction and the ascendency of the system. The difference between the harvested energy and the tive exergy flux can be allocated to increasing internally dissipated flux of a system is equvalent to its exergy the energy-intercepting biomass. The size of the flux.For more information see text. Redrawn with permission waterwheel paddles has been increased! Main- from Reynolds (1997a). taining more biomass carries a higher cost (it is shown as a linear function of biomass in Fig. 7.11)but, as more light-harvesting centres that are relatively most capable of overcoming the are placed in the light field begin to shade each effects of small inoculum sizes. Once again, r- other out, the harvesting return per unit invest- selected C-strategist species can be seen to hold a ment declines asymptotically. The limiting con- fitness advantage in aspiring to dominance. dition comes when the cost of maintenance can no longer be balanced by the harvested income Ascendency: environmental constraints and the exergy flux falls to zero. Some changes in community metabolism and Long before that condition is reached, ascen- resource partitioning through a phase of biomass dant accumulation is led by the recruitment accumulation in the Blelham enclosures (Section and expansion of species that contribute most 5.5.1;Fig.5.11)areillustrated in Fig. 7.12. The strongly to the aggregate biomass. These are not large panels summarise the variations in the necessarily the fastest growing (cf. Fig. 5.19)but, main contributing species to the phytoplanktic in the early stages of accumulation, the greatest biomass in the enclosure (Fig. 7.12b, as biomass rates of expansion are likely to come from the carbon) and their rates of population change fastest-growing oftheavailable pool and which (Fig. 7.12c: shading separates the reconstructed 358 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.12 Production and dynamics of phytoplankton recruitment in a Blelham Enclosure (A, 1983), during a period (a) of weak mixing (vide zm) and following high transparency (zeu) and artificial fertilisation with nitrogen and phosphorus. Changes in the biomass of prominent species of phytoplankton are shown in (b) on a common scale of carbon concentration. The rates of net population change (plus or, below the horizontal line, minus) are shown in (c), relative to reconstructed growth rates, after correcting net rates for grazing losses. Changes in the net daily photosynthetic rates, measured directly (P) and as the rate of cell recruitment by growth, before grazing and sinking (Pn), each specific to the upper 5 m of water, are shown in (d) (curves fitted by eye). Changes in the standing biomass (B)are shown, and similarly summarised in (e). Productivity trends (P/B, and especially, Pn/B), are shown in (f). Changes in the concentrations of SRP and DIN (= nitrate + ammonium nitrogen) (g) reflect uptake by the phytoplankton. Changes in the stock of phosphorus (TP) in the water column and its apportionment between soluble (SRP) and particulate (PP) components are shown in (h) together with the aggregate of phosphorus collected in sediment traps. Original data of Reynolds et al.(1985), as reworked and presented in Reynolds (1988c) and redrawn with permission from Reynolds (1997a).

growth rate from net rateofpositiveornega- irradiance, zeu). At the end of June 1983, the onset tive change), in relation to day-to-day variations of a phase of very stable thermal stratification in the depth of the mixed layer (zm)andthedepth coincided with the rapid depletion in the dom- of the conventionally defined photic zone (to 1% inant populations of Planktothrix (sinking and penetration of the immediate subsurface visible photooxidation) and Cryptomonas (to grazers) and ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 359 an attendant increase in transparency. The enclo- balance or exceed the rates of its recruitment, sure was then well fertilised with solutions of but shows well the increasing interference of the nitrate, phosphate and silicate. The responses of a major constraining forces on energy-harvesting now-diminished phytoplankton to this relatively and resource-gathering with the process of sharp increase in carrying capacity was followed recruiting new biomass. These effects carry other over the next two months, after which cooler interesting hallmarks of autogenic change in and windier conditions obtained. The changes to developing communities. The change in compo- the community during July and August are pre- sition, first in favour of strongly r-selected C- sumed to have been substantially autogenic (self- strategist species, such as Ankyra,towards slower- imposed), working within the limits of the con- growing, strongly K-selected, biomass-conserving straints of the carrying capacity of the light and S-strategist species such as Microcystis,isreflected nutrient resources. in the changing size spectrum of the popula- At the metabolic level, gross volume-specific tion (Fig. 7.13a). During early ascendency (take primary production (P,inmgCL−1 d−1)asindi- the windowfor15July), the major part of the cated by conventional radiocarbon fixation rates biomass resides in the smallest organisms: vir- (data of Reynolds et al., 1985)andphytoplank- tually all are individually smaller than 104 µm3, ton biomass (B,asmgCL−1)increased over the and over 50% of them are each less than 102 µm3). two-month period (Fig. 7.12d,e). However, produc- Towardsthe end of the accumulation phase (9 tion net of respiratory losses (Pn) and productiv- August and persisting until October), the major ity (sensu production normalised to biomass, P/B fraction is made up of units each >105 µm3. and, especially, Pn/B)decreased (Fig. 7.12 d, f). The Moreover, the distribution of biomass among increase in biomass took place at the expense of individual species also declines, with an increas- the nutrients in solution (Fig. 7.12g). Removal of ing proportion of the primary productive poten- dissolved phosphorus, ostensibly into phytoplank- tial of the community residing in the assembled ton, was effectively complete by early August, biomass of a decreasing number of species (Fig. while the general decline in the total phospho- 7.13b). The tendency is towards 1, as the best- rusfraction is explained by the sedimentary flux adapted species in the pool progressively outper- of planktic cadavers (mostly of the animals that forms, to their eventual exclusion, all the oth- had grazed on the phytoplankton). ers competing for the same, diminished resource. At the compositional level, the dominance of This is an issue not of species richness but of the phytoplankton changed twice – the leading species diversity, to which the discussion will contender for the opening resource spectrum was return (see p. 364). Ankyra, whose increase in biomass was initially supported by rapid net specific rates of increase Succession of ∼0.86 d−1 (reconstructed cell replication rates, Distinctive patterns in the developing meta- r ∼1.1 d−1). These were not sustained and the bolism and community organisation of major population was reduced by zooplankton feeding, biological systems, manifest as an ordered especially by filter-feeding Daphnia.Thesecond sequence (or succession) of substitutions of dominant was the non-motile colonial chloro- species, have long been recognised by plant phyte Coenochloris, whose net rate of increase botanists and geographers (Margalef, 1997). Early- (≤0.43 d−1)wasless sensitive to grazing but twentieth-century plant ecologists were espoused nevertheless weakened as zeu diminished in rela- to theidea of an internally controlled process, tion to zm. Microcystis increased steadily through culminating in a final, climactic stage of max- July and early August (≤0.24 d−1), achieving dom- imal persistent biomass. Moreover, some well- inance in place of Coenochloris.Its biomass per- characterised successions (for instance, from bare sisted, even though there was almost no net soil to high forest: or the hydroseral stages of recruitment from phytoplankton growth. vegetation development at the edge of a lake, The example illustrates not just the increas- passing from swamp to marsh or fen through ing burden of accumulating biomass, as loss rates to Quercus forest: Tansley, 1939)havesharpened 360 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.13 (a) The changing size distribution of changes wrought by the activities of individual phytoplankton in Blelham Enclosure A, traced through the organisms, to the extent that they alter the envi- allocation of the total live biomass among units (cells, ronment so that it becomes more amenable to coenobia or colonies) in the size categories shown. Note the theestablishment of individuals of other species, predominance of small cells (mostly of Ankyra)on15July, are, in broad terms, essential and predictable during the early part of the sequence depicted in Fig. 7.12, aspects of succession (Tansley, 1939). ‘Succes- and the predominance of larger algae later in the year. (b) The sion’ should be reserved to refer to these wholly changing apportionment of biomass among species, moving from being invested in the first two to four co-dominants to autogenic responses of the community (see also being almost wholly invested in the first. Original data of Reynolds, 1984b). Reynolds (1988c) and redrawn with permission from Successional changes, contingent upon auto- Reynolds (1997a). genic drivers, are the principal manifestation of ascendency in developing ecosystems (Odum, aresolve to find deterministic explanations. This 1969). We may accept ‘autogenic succession’ and quest has had to reject some well-intentioned but its attributes, as circumscribed by Odum (Table erroneously rigid statements of successional gov- 7.7), as being symptomatic of ascendency. Sev- ernance. At the other extreme, understanding of eral of the stated attributes plainly apply to the succession has not been helped by the use of this events depicted in Fig. 7.12.The ‘causes’ of suc- term by students of the pelagic to refer to all cession are the reactivity and interactions of the temporal changes in the species composition and pool of the species to the environmental oppor- the abundance and relative dominance of the tunities presented. It is these that may eventually plankton (Smayda, 1980). The fact that succession lead to structures that, subject to the turnover of ‘conforms to no plan’ and is mostly concerned resources, achieve a steady state of energetic bal- with the relative probabilities of certain possi- ance, to which the notion of successional climax ble emergent outcomes (Reynolds, 1997a), might is fully applicable. overcome the need for a precise explanation of its mechanics. Filtration and community assembly However, some aspects of the concept of suc- Where strict successional selection fails to cession are too valuable to reject. Change in com- explain the mechanisms underpinning repro- munity structure, in the plankton as in systems ducible sequences, then we need to invoke involving higher plants and animals, has a num- another model. The opposite view from posi- ber of quite separate drivers. These may owe to tive selection invokes the premise (see p. 351) allogenic,non-biological, physical forcing mecha- that most species can grow anywhere they arrive nisms (earthquake, fires, storms and floods) that at, provided the habitat is suitable and can destroy structure or modify the environment in sustain their growth and survival needs. Then, favour of tolerant species. On the other hand, the habitat that is, or becomes, unsuitable will ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 361

Ta b l e 7.7 Attributes of early and maturing stages of autogenic succession

Ecosystem attribute Early stage Maturing stage Community energetics 1. Gross production/community respiration (P/R)(P/R) >1(P/R) → 1 2. Gross production/biomass (P/B) high low 3. Biomass supported/unit energy income (B/Q)low high 4. Net production yield (Pn) increasing low 5. Food chains linear web-like Community structure 6. Total organic matter small arge 7. Inorganic nutrients extrabiotic intrabiotic 8. Species diversity rising high, possibly falling 9. Species equitability decreasing low 10. Biochemical diversity low high 11. Structural diversity poorly organised well organised Life histories 12. Niche specialisation broad narrow 13. Organismic size generally small generally large 14. Life cycles short, simple long, complex Nutrient cycling 15. Mineral cycling open substantially closed 16. Exchanges among organisms and environment rapid slow 17. Role of detritus in nutrient unimportant important Selection 18. Growth selection rK 19. Production for quantity for quality Community homeostasis 20. Internal symbiosis undeveloped developed 21. Nutrient conservation poor good 22. Response to external forcing resilient resistant 23. Entropy high low 24. Information low high

Source: Based on Odum (1969). simply select against the persistence of intoler- Then the organism can survive to the limits of its ant species. In this way, environments act as a own adaptive capabilities. These may be superior sort of filter, separating off the ill-adapted species or inferior to those of the next species and these from those whose traits and adaptations allow may well determine which of them can continue them to pass to survival. For instance, the poten- to function under persistently low oxygen con- tial of aquatic habitats to support aerobes is centrations. Pelagic environments pose many and constrained by a limited, finite supply of oxy- more subtle conditions and constraints to their gen. To be able to live in water, organisms are exploitation by aquatic organisms and the puta- required to be functionally or physically adapted tive systems to which their presence contributes. to ensure that diffusion gradients are adequate These may well operate simultaneously, as filters to theneeds that their size and activity dictate. of varying coarseness, to favour or disfavour the 362 COMMUNITY ASSEMBLY IN THE PLANKTON

Ta b l e 7.8 The rules of community assembly in the phytoplankton, proposed by the International Association of Phytoplankton Taxonomy and Ecology (see Reynolds et al., 2000b) with minor modiﬁcations

(1) Provided suitable inocula are available, planktic algae will grow wherever and whenever they can and to their best potential under the conditions obtaining. (2) Then, of those present, the species initially likely to become dominant are those likely to sustain the fastest net rates of biomass increase and/or to be recruited from the largest inocula (‘seed banks’). (3) The largest autochthonous inocula (seed banks) are furnished by species that have been abundant at the location in the recent past. (4) Environments may select, preferentially and with varying levels of intensity, for certain specific organismic attributes or traits. (5) Species with preferred attributes are likely to build bigger populations than those that lack them and, where appropriate, to found larger inocula to carry forward. (6) Plankton assemblages become biassed in their species composition by the conditions typically obtaining in the host water body. (7) The species most frequently present in specific environments share common suitable attributes. (8) The outcome of assembly processes may be subject to the food web and to other interspecific interactions. (9) Of those species present (and quite independently of the initial conditions), the ultimate dominant is likely to be the one most advantaged by its adaptive traits. (10) Assembly is always subject to the overriding effects of environmental variability and the resetting of the assembly processes.

relative abundances of each of the given species. of others (see for, instance, the papers of Belyea The most decisive of these criteria becomes the and Lancaster, 1999;Brown, 1999;Straˇskraba finest of the filters operating, selecting for the et al., 1999). Here again, the value of the short fittest of the species available (Reynolds, 2001a). timescales of community processes in the pelagic In this way, the fortuitousness of the species have permitted the substantial verification of the composition of the various functional compo- role of trait selection in the development of nents of a community and the stochastic nature pelagic communities (Rojo and Alvares Cobelas, of its early dominance is squared against the 2000). A definitive set of rules guiding the assem- increasing predictability of the outcome of auto- bly of communities in the plankton has been progenic succession. The mechanisms have yet to be posed by the International Association of Phyto- fully elaborated. My use of the word ‘filtration’ plankton Taxonomy and Ecology (see Reynolds et (Reynolds 2001a)wasinspired by the reference al., 2000b)(seealso Table 7.8). These repeat some of Lampert and Sommer (1993)to‘environmen- statements offered earlier in this chapter. tal sieving’. However, the crucial role of specific It has already been established (Chapters 5 organismic traits in, as it were, determining the and Sections 7.2.2 and 7.2.4)that the principal filterability of species that may then participate correlatives of community composition are clas- prominently in community function is provided sifiable as resource constraints and energy con- by the seminal work of Weiher and Keddy (1995; straints (e.g. Fig. 7.8). It is now a simple exer- see also Weiher et al., 1998). Their formulation of cise to suggest the assembly mechanisms under- the guiding principles and rules governing com- pinning the distribution of trait-distinguished munity assembly has attracted the concurrence functional groups against these constraints. The ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 363

(shown by hatching) of most planktic species present. Thus, they furnish an ascendent opportunity, unconstrained save by their own exploitative capabilities. Interspecific competition for the opportunity is weak but, in accord with Rules 1–3 (Table 7.8), the species that become most prominent will be the ones generating the highest exergy and investing in the fastest relative ratesofgrowth. Working downwards to Fig. 7.14b, reduction of the base of the potentially critical nutrient to growth-limiting levels (Section 5.4.4) demands traits of high uptake affinity for the limiting nutrient, or the ability to exploit other less-accessible resources, which may be shared by relatively few of the contesting species. Once nutrient is exhausted from the upper column, theonly exploitable resources are located deep in the light gradient (Fig 7.14c), requiring yet greater Figure 7.14 Idealised environments, defined in terms of specialist organismic traits to be able to use them downwelling solar irradiance (I) and the capacity-limiting and, therefore, fewer species able to compete for bioavailable resource (K)inrelation to mixed depth them (Rules 5, 6 and 9). (represented by the temperature gradient (θ). The potential Working rightwards in Fig. 7.14,the light- biomass and its distribution is shown by shading. In the top left diagram (a), resources and, at the top of the water harvesting opportunities are diminished by weak- column, growth is saturated at the maximum potential of the ening stratification and increased mixing depth. producers present. Working downwards, many water Light-harvesting opportunities are diminished in columns correspond to (b), wherein resources are so scarce consequence, although they are extended and or depleted that they constrain the productive potential, renedered more uniform through the entire possibly as far as to the metalimnion (c). Working rightwards, mixed layer (Fig. 7.14d). Ascendent biomass also deeper mixing (d) relative to diminishing light penetration (f) impinges increasingly upon light penetration: sets the major functional constraint. Most systems probably increased depth of mixing and raised turbidity fluctuate around a condition close to (e) but the inference of levels impose greater adaptive efficiency of the deep mixing and nutrient deficiency (g) as being untenable to primary producers is clear. Based on an original figure of light-harvesting apparatus and enhanced ability Reynolds (1987b) and redrawn with permission from still to cream off the remaining exergy genera- Reynolds (1997a). tion into biomass accumulation (Fig. 7.14f). It has to be said at once that these are idealised states, none of which obtains constantly. representation of pelagic habitats shown in Fig. Real systems show variability in both directions 7.14 is now well travelled and a little dated but it and may hover around conditions represented by serves to illustrate how temporal habitat changes Fig. 7.14eHowever,theinference of simultane- in light and nutrients intensify species filtration ous segregation of the nutrient base from the of species traits. The individual subfigures (a–g) energy-harvesting opportunity is supports only a making up Fig. 7.14 represent vertical profiles of desertified habitat (Fig. 7.14g), corresponding to light availability (I)andnutrient concentration temperate oceans in winter (Fig. 1.8). (K), in relation to temperature (θ,included in this The arrangement in Fig. 7.14 also picks up the instance only as a correlative of structure and ver- layout of the C–S–R triangle, serving to amplify tical mixing). In the first instance (Fig. 7.14a, in both the conditions and (for fresh waters) the the top left-hand corner), nutrients and, at least notional ranges of some of the trait-distinguished near the surface, light, are shown to be capable of functional groups (cf. Figs. 7.8, 7.9). For systems saturating the immediate growth requirements that are chronically resource-deficient (K∗∗ always 364 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.15 The impact on ecosystem energetics of chronic resource deficiency and low energy income, based on Species richness, diversity and evenness in their representation in Fig. 7.11. The basic layout is shown as assembling communities being constrained by axes delimiting low or variable Recalling the representation of seasonal varia- resources or energy income, which, respectively reduce the tions in environmental selectivity for a given exergy to the smaller shapes in (b) and (c). The preferential individual water body (Fig. 7.9), the C–S–R trian- trend towards S or R dominance is predicted. Redrawn with gle can be used to match the successional tra- permission from Reynolds (2002b). jectories of favoured species (or at least their respective trait-selected groups) to the extent and low) or, equally, in which harvestable light (I∗∗)is direction of environmental variation. Some well- habitually diluted by mixing or by turbidity, the documented pathways are plotted in this mode selective bias is strongly pressed against C strate- in Fig. 7.16,relating compositional changes to gies and towards those of either S or R species. thedrift in nutrient and light availability con- Moreover, the bias of inocula serves as a positive sequential upon community ascendency. This is feedback to influence the floristic composition of not prescriptive but purely an example of the the respective habitats. kinds of self-imposed ‘decision points’ that may The link to the assembly of communities in steer the assembling community towards par- these habitats is also simply represented through ticular outcomes. Starting at a point X, repre- referencetoFig.7.12.Ifwetakethe segment senting initially non-limiting nutrients and light, enclosed by the curves representing potential theassembling community is more likely than harvest over cost as the potential for ascendent not to be founded upon the primary production investment and subject it to persistent but vari- of relatively fast-growing, r-selected nanoplank- able constraints in either energy or resource, tic species of one or other X algal associations. two new shapes may be derived income (Fig. Early dominance of these organisms is not bound 7.15a). Chronic resource limitation of supportable to collapse: two possibilities for perpetuation are biomass lessens the likelihood of frequent limi- included in Fig. 7.16, where dilution by nutrient- tation of growth by harvestable light (Fig. 7.15b). rich throughflow (‘FLUSH’) and avoidance of con- High exergy can be maintained by species that sumers (‘NO GRAZE’) permit the endurance of the cope with resource limitation (and are highly sen- status quo,provided nutrients and light remain sitive to altered loadings of critical nutrient). For freely available. Modest, delayed or selective graz- systems that are energy-limited, the biomass is ing in water columns sufficiently deep to be unconstrained by nutrient whereas it can rise to subject to self-shading may operate in favour the level of the limit of theexergyharvest by the of self-regulating cryptomonads or (eventually) most efficient users of the available light (Fig. of efficient energy harvesters such as attenu- 7.15c). The respective selective biasses in these ate diatoms and filamentous Cyanobacteria. The extremes favour S-andR-strategist species. greater becomes the light constraint, the more ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 365

Figure 7.16 Some pathways in the development of phytoplankton composition, with some key ‘decision nodes’. Starting at X, the predicted initial establishment of r-selected, invasive C-strategists may be perpetuated by flushing or may otherwise persist if there is no grazing. Early imposition of grazing may force the dominance of sequences of larger and, eventually, more versatile phytoplankters (Eudorina → Ceratium); otherwise, diminution in light availability pushes dominance towards energy-efficient R-species. If resources are not replaced, or are chronically deficient, sequences move vertically towards specialist resource-gleaners and, possibly, to the dominance of picophytoplankton. The enclosure within a triangle ties these temporal patterns to the habitat template. Redrawn with permission from Reynolds (1997a). intense is the competition for the available pho- pressure in favour of the late successional par- tons, the tighter is the filter and the less is the ticipants and against the weaker competitors for diversity of still-functioning species. The model thecritical resource. The system moves towards reconstructions of increasing light constraints on asteady state, because its rate of building and the comparative growth rates of Chlorella, Asteri- thecost of its maintenance are balanced and, onella and Planktothrix also amply predict this out- forsolong as the constraints remain, no bet- come. ter competitor is available to contribute new Alternatively, the early onset of heavy grazing exergy. The community has, in fact, achieved is likely to work against self-shading and directly its potential, analogous to its successional cli- in favour of larger algae. Comparative growth max (Reynolds, 1993b, 1997a;Naselli-Flores et al., rates, inoculum size and the relative intensity 2003). The outcome is not altogether random: of developing constraints in the resource sup- theoverwhelming dominance of the best comply (phosphorus, nitrogen and carbon flux) each petitor for the most severe constraint may be influence the compositional trends among these anticipated, in part, from a knowledge of the algae (whether as a consequence of high affinity properties of the habitat (deep or shallow, hard- for phosphorus, the metabolic flexibility to fix or soft-watered, phosphorus-rich or phosphorus- nitrogen or to resort to mixotrophy, mobility to poor). However, the outcome is fashioned entirely glean orscavengetheresources available or the by theassembly process. Community develop- ability to enhance carbon uptake). The greater ment pushes the selective pathway towards one becomes the particular resource constraint, the or other of the selective apices (S or R in Fig. 7.9), more important are the specific means of its where the growth of only a few specialist-adapted retrieval. Again, the filter tightens and the num- species remains possible. It is as if the richness ber of (increasingly S-strategist) species still able of species potentially able to contribute to the to function diminishes. In this way, the develop- late stages of community assembly is increasingly ing interactions increasingly exert the selective ‘squeezed out’ as the apices are approached. The 366 COMMUNITY ASSEMBLY IN THE PLANKTON

patterns analysed in Section 7.2 and, especially, have acknowledged, will be extremely rare. Thus among some of the mesotrophic and eutrophic the value of s becomes partly a function of the lakes (Section 7.2.4)provided several examples of diligence of search and it is likely to be influ- quasi-steady states of extended dominance by one enced by the taxonomic competence of the asses- (or a very small number of) persistent species. sor. Students of phytoplankton elect to adopt a These are, moreover, considered to be typical for cut-off (generally, though quite arbitrarily, that the particular conditions in particular groups they will include only those species each con- of lakes. These include the sequences culminat- tributing >0.5% of B)that immediately weights ing in long phases of dinoflagellate dominance thediversity indices they quote against the rare of nutrient-depleted epilimnia (Peridinium in Kin- species in their original samples. This being so, neret, Ceratium in Rostherne Mere); the forma- thevalid measure that should be sought is the tion of deep chlorophyll maxima in stable metal- equitability (or evenness) of the species represen- imnia (as Planktothrix rubescens in Zurichsee);¨ the tation (Es), which approximates to: association of dominant populations of Anabaena = / spp. or Cylindrospermopsis with hydrographically E s H Hmax (7.5) stable periods in N-deficient tropical lakes (see p. 344); and the near-perennial dominance of Scores for equitability are rarely quoted, partly highly enriched, shallow polder lakes by Plankto- because the difficulties of estimating s persist. thrix agardhii and/or Limnothrix redekei (pp. 345, Thus, the calculated diversity indices (H)that are 349). usually quoted provide only a proxy estimate of There may be little doubt about the domin- the course of temporal changes or between-site ance but competitive exclusion of less-fit species comparisons of community organisation. There by those more adaptable is rarely so complete have been other, less well-used approaches to that small numbers of excluded species or (espe- capturing mathematically the drift in species cially) their propagules do not persist within the equitability. For instance, Margalef’s (1958)index system for many years. Here, they constitute a of diversity, Hs,simply relates the number of sort of system ‘memory’, whence they may, fol- species (s)tothetotalnumberofindividu- lowing some future environmental modification, als (N). Applied to a fixed size of sample (vol- have the opportunity to reassert their abundance ume of water), the diligence-of-search criterion (Padisak,´ 1992). Species richnessisthusalesssen- is cut off in an arguably less arbitrary way. How- sitive barometer of the structural organisation ever, it has a transparent sensitivity to increased of communities through succession than is the biomass and the number of species that are relative distribution of the biomass among the common. The units are bits (of information) per species present. individual: Ecologists express the diversity and equitabil- = − / ity (or evenness) of species assemblages using Hs (s 1) loge N (7.6) termsborrowed from Shannon’s (1948)theory of information. Pielou (1975)proposed that the Margalef’s index is used to construct the quan- most useful estimate of biotic diversity (H ) tified analogy to the changes in species even- comes from the specialised form of the function ness through the summer accumulation phase (from Shannon and Weaver, 1949): in a Blelham enclosure (Section 5.5.1)(Fig.5.11) and the progressive onset of Microcystis domi- H =−b /B log (b /B )(7.4) i 2 i nance through exclusion, shown in Fig. 7.17. where B is the total biomass, and bi is the biomass The observed changes in contributory specific of the ith of the s species present. H increases biomass (shown in the upper part of the figure) with the number (richness) of species. Thus, we and the rates of community change (σ s), calcu- should expect the biotic diversity to be a contin- lated over 3- to 4-day intervals are included for = uous function of richness, such that Hmax log2 comparison. The latter is calculated, according to s. The majority of the those species will, as we Equation (7.7), based on the original derivation of ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 367

in a steady state of overwhelming dominance, reflected by a very low rate of community change −1 (σ s < 0.03 d ), any residual evenness is lost. In spite of the implicit shortcomings of the Shannon–Weaver index, it continues to be much themore commonly used. Moreover, experience indicates that the application of the cut-off reveals very well the change in individual species contributions to biomass through the course of succession. For instance, it is a well-attested principle that, in a fully operational ecosystem, ‘most’ (≤95%) of the biomass at each functional level (primary producer, herbivore, decomposer, etc.) is accounted in the first six to eight species (Hildrew and Townsend, 1987). In my own career experience of counting upwards of 6000 individual samples of phytoplankton from lakes, reservoirs and rivers, I have never encountered one in which more than 20 species were simultaneously represented at >1 cell mL−1,orbymorethan 60 species exceeding 10 L−1. This is despite the fact that, in some cases, the full list of recorded species at the various given locations has exceeded 150. In the many cases where cell counts were transformed to biomass, there has not been one instance in which the eight most abundant species made up <95% of the total standing mass of the phytoplankton crop. Indeed, the 95% threshold is frequently surpassed by just one to three of the most Figure 7.17 Periodicity of dominant phytoplankton in abundant species. So it is that, even within a vari- Blelham Enclosure A in 1982. From changes in the relative abilty range of the one to eight species that will abundances of each species shown in (a), the rates of typically comprise ≥95% of the mass of phyto- σ community change ( s) and community diversity (Hs)are plankton, the truncated Shannon–Weaver index calculated and plotted in (b). Redrawn with permission from is perfectly sensitive to variations in the compo- Reynolds (1997a). sitional diversity. Examples of its use are cited in the following section. a‘succession rate index’ of Jassby and Goldman (1974b): 7.3.3 Species diversity and disequilibrium in natural communities σ = {[b (t )/B (t )] − [b (t )/B (t )]}/(t − t )(7.7) s i 1 1 i 2 2 2 1 High diversity is a feature of many biological sys- where B is the total biomass and bi is the biomass tems and itisgenerallyconsidered to be impor- of the ith species on each of two occasions (t1 and tant for their healthy functioning (Reynolds and t2), so that σ s is averaged over the period that sep- Elliott, 2002). Whether this is always or only arates them (units, d−1). The plot in Fig. 7.17 con- sometimes true, high species richness, equitabil- firms the increase in the number of participating ity and genetic representation are believed to be species in the early phases (Hs: 1–2 bits per indi- under threat and, therefore, worthy of conserva- vidual) and that diversity is kept up while species tion (Lawton, 1997). It follows that the ‘protec- composition varies considerably (σ s: 0.1–0.3 tion of biodiversity’ must be a good thing, even d−1). Once Microcystis becomes abundant and if there has been an incomplete understanding 368 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.18 Time courses of Margalef’s diversity index in the mesotrophic North Basin of Windermere, the eutrophic Crose Mere and the well-fertilised Blelham Enclosure B during 1978. Redrawn from Reynolds (1984a).

of just what this means, much less any clear well-fertilised Blelham Enclosure (Fig. 7.18)was strategy for bringing it about. Biodiversity (origi- used by Reynolds (1984a)toillustrate the then nally BioDiversity, coined as a shorthand for Bio- general belief that lake systems maintaining high logical Diversity: Wilson and Petr, 1986) has no nutrient availabilities support poorer species precise definition and it has no units of mea- diversities than oligotrophic systems (Margalef, surement. As a synonym for ‘species richness’, it 1958, 1964;Reynolds, 1978c). This point now can assume fairly precise terms but it is either requires further discussion (see Section 7.3.3 reliant on a sophisticated and continuously accu- below) but Fig. 7.18 presently serves to show that mulating knowledge base of how many species thelow values observed in the Blelham Enclosure −1 there are. Atthesametime, this understanding Bin1978 (Hs 0.24–1.75 bits individual ) had not requires an area-based focus. For instance, there been dissimilar from those noted in the Enclo- is (presumably) a finite number of species on sure A in 1982 (Fig. 7.17). The differences between the planet, each with an instantaneously finite themeasures for the eutrophic Crose Mere (Hs number of individuals; elimination of these is 2.00–4.15) and the mesotrophic North Basin of −1 to extinguish the species. On a regional or local Windermere (Hs 1.78–6.44 bits individual )are basis, the extinction of species may be reversed generally small but for the wide departures in by subsequent invasions of new individuals of thesummer months. These may be compared the same species from remote populations. It also with Margalef’s (1958)ownassessments of seems important to establish the mechanisms diversity in samples taken from the Ria de Vigo, maintaining high local species diversity, again through the summer progression from diatom to through reference to (apparently) cosmopolitan dinoflagellate dominance (Hs 0.8–5.4) (see p. 311 species whose short-generation organisms render and Fig. 7.19). Recent studies of phytoplankton thetimescales of exclusion and dispersal conve- diversity among a broad range of European lakes niently measurable. quote seasonal fluctuations in Shannon diversity Phytoplankton assemblages in natural lakes (truncated H values) in the range 1–3.5 in strat- and coastal waters often comprise several main ifying lakes (Leitão et al., 2003; Salmaso, 2003), species simultaneously and these contribute to or slightly higher (2–5) in shallow lakes (Padisak,´ relatively higher measures of ecological diver- 1993;MischkeandNixdorf, 2003). sity, as measured by the Margalef or trun- Hutchinson (1961)famously drew attention cated Shannon–Weaver indices, than is suggested to theparadox that high diversity among phy- by the plot of Hs in Fig. 7.17 for anexperi- toplankton species competing for essentially the mental enclosure. The plot comparing diversity same limiting resources in an apparently homo- indices from Windermere, Crose Mere and a geneous environment is counter-intuitive and ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 369

Figure 7.19 Variations in the index of diversity in a number of samples of phytoplankton collected from surface waters of the Ria de Vigo in 1955 plotted against the successional stages diagnosed by Margalef (1958). Redrawn with permission from Fogg (1975).

against Hardin’s (1960)principle of competitive to grow and increase specific biomass under exclusion (see also Box 7.1). Since that time, tolerable environmental conditions but which there have been numerous attempts, often with show a net loss of biomass under conditions as compelling experimental evidence, to argue they become intolerable. Just the simultaneous forasatisfactory explanation. These broadly occurrence of species whose numbers are increas- divide among three categories. Following Paine ing while those of another are in net decline (1966), species coexistence is promoted primarily is sufficient to maintain species richness and through food-web interactions. Following Tilman local species diversity throughout the period that (1977)andothers, coexistence reflects simulta- the two sets of responses can be detectable. For neous, niche differentiation of the surviving this reason, low diversity (H ,Hs)mustalways species. Disciples of Connell (1978) attribute a be accompanied by low rates of compositional rich biota to temporal and simultaneous spatial change (σ s). Equally, the maintenance of high variability of the environment. These explana- diversity must be viewed within the context of tions are not mutually exclusive and, indeed, time constraints set by changing rates of popula- they may besummative. However, the impor- tion recruitment and attrition. tance of the topic requires ustoexaminethe The time-frame of ecologically relevant mechanics of these concepts in more detail. responses to an infinitely variable environment is supposed to be bounded (at the lower end) Disequilibrium by thegeneration time of the shortest-lived Hutchinson’s (1961)ownexplanation of the para- species and (at the upper) by the time taken to dox lay in the error of the first assumption reach a competitively excluded climactic state of environmental homogeneity and steady-state (Reynolds, 1988c, 1993b). Smaller-scale variabil- conditions. In all the examples considered in ity may demand reactivity at the biochemical this chapter, species composition is shown to and physiological levels. Provided that the cell change conspicuously through time. In every can maintain its cycle of growth and mitotic instance, this is shown to be driven by a bal- division, the variability is smoothed to ecolog- ance of dynamic responses of planktic species ical constancy. Environmental changes outside that have ‘arrived’ from elsewhere, that are able theperiod of ascendency to climactic steady state 370 COMMUNITY ASSEMBLY IN THE PLANKTON

that may destroy biomass and precipitate a new eventually averaging 700–1000 cells mL−1. These potential climax – such as inundation of vegeta- maxima, observed in late August or early Septem- tion by a marine incursion or the desertification ber, arise almost exclusively, through serial divi- of forest to scrub – have intrinsic interest but tell sions, from a base inoculum of excysting overwin- us little about successional maturation. tering propagules of between 0.1 and 1 cells mL−1, Against the many scales of physical variabil- recruited to the water column in February. The ity in aquatic environments (Sections 2.1, 2.2.2, 11–14 doublings required to achieve this occupy 2.3.2, 2.3.3), the timescales of phytoplankton pop- around 200 days, although the fastest rate of ulation ecology are readily discerned. The maxi- increase is generally attained during July (∼0.15 mum growth rates of the weedy and more inva- d−1, coinciding with the warmest water, longest sive C-strategist phytoplankters – exemplified by days and nutrients still not limiting). The obser- Chlorella and Ankyra – have standardised specific vations are comparable with those for Esthwaite −1 replication rates (r 20)of>1.8 d in culture Water ofHeaney et al.(1981) and the growth rates (Table 5.1). Verified field growth rates of 1.1 d−1 observed in attaining smaller maxima in the Blel- (Table 5.4)bring the potential time of biomass ham enclosures (Lund and Reynolds, 1982)(see doubling to matter of several hours (certainly to also Fig. 5.18)arealso comparable. <1dunder ideal field conditions). Of course, Several summer maxima in the Blelham progress may well be impeded by the interven- enclosures, similarly achieving concentrations tion of poor average light conditions, nutrient equivalent to >600 mg chla m−2 (>30 C m−2), exhaustion or grazer responses and be truncated have been overwhelmingly dominated by Micro- farshort of a climactic steady state. Physical fac- cystis populations of 300 000–400 000 cells mL−1. tors are alsoimportantbut rapid flushing rates Again the initial recruitment has come from may benefit fast-growing organisms over slower small colonies that entered the plankton between species and their consumers. However, an ade- April and June (see Section 5.4.6). Sustained expo- quately discretionary rate of dilution leaves the nential growth during the summer (rn between net rate of population increase only just positive 0.15 and 0.24 d−1, slowing towards the end) and thus the attainment of the potential pro- would raise an invading the standing population vided by growth is much protracted. The physi- from the equivalent of 100–200 cells L−1 to its cal conditions suspend the advance of the suc- maximum through some eight or nine genera- cession, maintaining it in a sort of plagioclimax tions in about 5–8 weeks of growth. Prior to that, (Tansley, 1939). Elsewhere, selection through the three or four divisions of the overwintering cells foraging preferences of the zooplankters present contributing the invasive colonies whilst still forparticular foods or particular particle sizes, on the sediment perhaps needs to be included constraints in the availability and accessibility of (Preston et al., 1980;Reynoldset al., 1981). resources and light all affect the relative success It was these considerations that allowed of the tolerant species in moving towards dom- Reynolds (1993b)topropose that the period inance. A phase of apparently enhanced coexis- required for a phytoplankton succession to move tence and (thus) higher measurable diversity is from initiation to a competitively excluded cli- passed before the strongest competitor eventu- max is equivalent to some 12–16 generations. ally emerges as the dominant species of a low- Given favourable conditions and the resource diversity climax. capacity to sustain it, the entire process might We have considered examples of Ceratium, occupy 35–60 days. Microcystis and Planktothrix moving to this stage However, it is also plain that, in the plankton of community development. In Crose Mere (Fig. as on land, such low-diversity climactic, steady 7.6), Ceratium has several times been observed states are exceptional occurrences. That diversity (Reynolds 1973c, 1976a)tobuilduptoasta- is normally kept high is seen to be largely a ble (low-σ s), low-diversity (Hs ∼2.0) maximum of consequence of processes that prevent, or delay, between 150 and 250 µgchla L−1 (∼900 mg chla perhaps indefinitely, the progress to the poten- m−2, ∼45 mg C m−2), comprising concentrations tial steady state. Communities remain, in fact, in ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 371 various states of ecological disequilibrium, hav- d−1)increases while alga B (r ∼0.1 d−1) decreases ing a persistent tendency to move towards a given when both are subjected to a filter-feeding con- (though possibly changing) climactic outcome sumerZ(F = 0.15 d−1). Food selection increases but in which progress is seriously impeded or the benefit to the ungrazed alga C (r = 0.1 d−1). stalled. In many instances, diversity and species The possibilities increase greatly if depth distri- richness are quite unrelated to trophic state and butions of food and feeder are considered; alga productive capacity (Dodson et al., 2000). Bmay now increase faster than A if B swims to thesurface while A fails to avoid the down- Internal (biotic) mechanisms of coexistence ward migrations of Z. Then the effects are again The activities of heterotrophs (principally, but multiplied if consumers X and Y feed on larger not exclusively, phagotrophs) within the same or smaller foods than Z or show particular pref- system interact with the population dynamics erences for a given alga. Finally, the growth of phytoplankton in a variety of ways. Easi- dynamics of algae and feeders are themselves est to understand is the concept of zooplank- fluctuating. It is not difficult to recognise the ton feeding indiscriminately on phytoplankton. complexities of phytoplankton interactions with By removing individual phytoplankters from the phagotrophs or how their fluctuating fortunes pool, even light grazing surely delays succes- contribute to the maintenance of diversity to the sional progress. It is theoretically possible that extent that Paine (1966)indicated. individual food organisms might be removed Phagotrophic grazers are not the only organ- at the same rate at which they are recruited, isms that influence the structure of the planktic which would ensure zero instantaneous rates assemblage from within (i.e. autogenically). Para- of advance. However, such balances are rarely sites and pathogens are generally highly specific struck (well-nourished zooplankters increase in in the algae they affect and it is frequently the size and recruit further generations of indi- most common (or recently most common) that viduals). The more common outcome is that attract epidemics (see Section 6.5). The progres- zooplanktic animals (at least, the filter-feeders; sive intervention of chytrid fungi was responsi- see Sections 6.4.2, 6.4.3)drawdowntheir foods ble for breaking the years of summer dominance to concentrations at which their own popula- of Ceratium in Esthwaite Water, and for accord- tion growth is impaired. The intervention of a ingly raising the subsequent diversity of the phy- third trophic component with a relatively slow- toplankton (Heaney et al., 1988) (see also Section changing impact intensity (such as planktivorous 6.5.2). fish or invertebrate species) is usually necessary to impart a simultaneous top–down regulation Resource competition as a mechanism of on zooplankton consumption (Reynolds, 1994c). coexistence The interactions among the consumers of the The theory of resource-based competition devel- microbial food web (nanoflagellates, ciliates) with oped by Tilman and co-workers (Tilman, 1977; theproducers (picoalgae, bacteria) are presumed Tilman et al., 1982) (see also p. 197)proposed an to place mutual constraints on the dynamics of elegant explanation of species coexistence and each other in a way that helps to ensure the assemblage diversity, invoking internal responses simultaneous survival of each of the components (specific resource uptake and growth rates) to (Riemann and Christoffersen, 1993;Weisse, 2003). external drivers (resource availability). The exper- Zooplankton grazing on phytoplankton is gen- iments of Tilman and Kilham (1976) showed how erally more selective in its effect. This selectiv- it was possible for two species of diatom to grow ity has several dynamic components that need simultaneously (and, hence, to coexist) for as long to be distinguished. Just the difference in the as one of them remained limited by the sup- replication rates of two phytoplankton species ply of phosphorus and the other by the supply may determine the relative success of one over of silicon. They reasoned that while they were the other whilst both are simultaneously grazed not in direct competition for limiting resource, by the same consumer species. Alga A (r ∼0.2 their coexistence would endure. Moreover, if two 372 COMMUNITY ASSEMBLY IN THE PLANKTON

species may coexist while each is independently limiting resources are thus able to maintain resource-limited, the further corollary is deduced larger inocula. On the other hand, the effective that there may be as many coexisting, non- exhaustion of a limiting nutrient, by species of competing species as there are simultaneously all affinities, means that the most likely outcome limiting factors (cf. Petersen, 1975). The high- of algal activity is that the uptake capacity for est species diversities, accordingly, might be the limiting resource is insufficient to support expected in environments of general resource further population increases. Ultimately growth, deficiency and, hence, the greatest likelihood of then cell division (r)isbrought to a halt, and simultaneous rate limitation. population change (rn)falls to zero or is negative. There is no shortage of experimental infor- Competition may certainly be keen but the rates mation to support the differentiation of interspe- of succession and exclusion are reduced to very cific growth rates along resource-ratio gradients. low values. It follows that species richness and Rhee and Gotham (1980)demonstrated analogous diversity endure because the mechanisms that performance differences among various common work against them are themselves severely con- species of phytoplankton with respect to the ini- strained. The low-diversity steady state is simply tial relative availability of nitrogen to phospho- postponed. rus, while Bulgakov and Levich (1999)cited exper- It must be noted that this logic does not inval- imental evidence in support of the widely held idate resource competition as a direct mecha- supposition that a low N : P ratio favours the dom- nism for sustaining coexistence, provided that inance of Cyanobacteria. Sommer (1988c, 1989) the turnoverofthelimiting resources, between has argued for competitive interactions among organisms and the labile pool, is demonstrably algae for diminishing levels ofSi,NandPfavour dynamic. Possibly the clearest evidence for this the seasonality of assemblages in kataglacial is the widespread co-dominance of ultraoligo- lakes (see p. 338). The important role of carbon trophic plankton assemblages, both in the open and its photosynthetic fixation is brought into ocean and in lakes, by nutrient-deficient photo- theappreciation through the ratios of light to autotrophic picoplankton and carbon-deficient nutrient and C : P availabilites (Sterner et al., 1997) bacterioplankton. The carbon (especially) is (see p. 199). rapidly exchanged through a labile DOC/DIC pool At first sight, simultaneous multiple limita- whereas carbon and nutrients are turned over tion is an attractive basis for explaining coex- by consumers of the microbial web. There is a istence. On the other hand, it is losing favour thus a near-continuous, differentiating compe- except in qualified circumstances. This is partly tition among the components and it maintains because simulation models of the dynamics of an ambient, diverse steady state. In these terms, multiple species limitations have not borne out the independent introduction of the erstwhile the prediction of stable coexistence but, rather, limiting nutrient is bound to help the photoau- have pointed to instability and chaotic outcomes totrophs rather more than the chemoautotrophic when more than two species compete for more bacteria, which will experience continuing severe than two limiting resources (Huisman and Weiss- or intensifying carbon deficiencies. ing, 2001). However, some of the experimental conditons and assumptions do not necessarily Disturbance as a mechanism of coexistence obtain in natural environments. As has been The third category of processes that pro- pointed out previously, resources either saturate mote interspecific coexistence is rather gener- the sustainable growth rate of phytoplankton or ally referred to as disturbance.Disturbances are they fall to levels that interfere with the abil- imposed by external (allogenic) forcing factors ity of just about all species to maintain a finite and are recognised by their effects in variously rate of growth (Section 5.5.4). Persistent low lev- delaying, arresting or diverting successional els of nutrients favour species with relatively sequences from achieving their low-diversity, high uptake affinities over species having weaker steady-state climaxes. Commonly cited types of affinities and to which the same resources are terrestrial disturbance include geophysical events unavailable. Species with higher affinity for (landslides, lava inundations) and abnormal ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 373 weather conditions (hurricanes, floods, droughts: hypothesis (IDH). In essence, it anticipates Sousa, 1984). In the pelagic, the best-known dis- that: turbance events are associated with hydraulic (1) In the absence of any disturbance, compet- or hydrographic disruptions of the water col- itive exclusion will eventually reduce the umn (flushing, strong mixing) or with nutrient number of surviving species to minimal lev- pulsing (Sommer et al., 1993; Sommer, 1995). els. Forexample, significant wind-mixing events dur- (2) At high frequencies of intense disturbance, ing summer in a small, stratifying, eutrophic only pioneer species are ever likely to re- lake (Crose Mere) were several times observed to establish themselves in the wake of each cut across the usual G → H → L sequence M disturbance. of dominant algae by restoring growth con- (3) If such disturbances are of intermediate fre- ditions suitable for diatoms (Reynolds, 1973a, quency or intensity, there are more and 1976a). The species that grew had been repre- longer opportunities for community ascen- sented in the vernal bloom (Association C;see dency and a greater variety of species will Table 7.1)butothers were confined to such sum- establish in the wake of each disturbance mer growths (notably Aulacoseira granulata,since but these will rarely be allowed to mature ascribed to P). However, in the post-disturbance to competitively excluded steady states. relaxation, a tendency for the G and H elements to recapitulate their post-stratification sequences The obvious consequence is that a peak of diver- was noted. Inthehighly disturbed early sum- sity should be found at intermediate frequencies mer of 1972, diatoms, G-chlorophytes and H- and intensities of disturbance. Cyanobacteria were maintained as co-dominant This is an elegant theory: its development is species (Reynolds and Reynolds, 1985). Later logical and its statements are intuitively correct. on, artificial mixings applied to the Blelham It has long remained a hypothesis for it is dif- Enclosures imitated these effects experimen- ficult, in most ecosystems, to collect appropri- tally (Reynolds et al., 1984). The imposed delay ate data to support or confound it. Planktic sys- to thesuccessional maturation, whilst retain- tems provide an exception to this statement, ing extant mid-successional populations and where successions from the establishment of pio- periodically resurrecting pioneer species, helps neer communities through to their total eclipse to bolster the diversity of the phytoplankton by steady-state, competitively excluded climaxes represented. can be completed potentially in under 60 days In this way, the impact of disturbance (see p. 370). It may be deduced, incidentally, that on diversity is related to the intensity and, theequivalent of 12–16 generations required for especially, the frequency of the forcing events potentially climactic tree species (with genera- (Polishchuk, 1999). However, the scales of impact tion times of 200–800 years) to achieve anything and timing have to be judged against the gen- closely resembling a competitively excluded cli- eration times and succession rates of the main max will occupy 2.5–100 ka. This represents is species involved (Reynolds, 1993b). Without the asubstantial fraction of an interglacial period. context of successional processes, understanding Given the reconstructed climatic variability over of the complex mechanisms underpinning the even the last ten thousand years (10 ka) since the diversity–disturbance relationship has been last great glaciation, the history of the chang- rather slow in development and not without ing dominant vegetation of the northern land controversy (Wilkinson, 1999). Even now, the masses (e.g., Pennington, 1969)maybelegiti- mechanisms are widely misunderstood, despite mately comparable to the periodicity of phyto- thefact that most of the relevant theory was plankton in a small temperate lake during a sin- in place in the mid-1970s (Grime, 1973;Foxand gleyear (Reynolds, 1990, 1993b). Connell, 1979). The work cited most frequently is As has also been pointed out on many previ- that of Connell (1978) whose strictures on species ous occasions, phytoplankton successions are not diversity in rain forests and coral reefs led to him merely observable but are amenable to practical to propose his memorable intermediate disturbance experimentation. IDH has been invoked in the 374 COMMUNITY ASSEMBLY IN THE PLANKTON

explanation of periodic sequences of phytoplank- Juhasz-Nagy,´ 1993 is most apposite), the litera- toninnatural lakes and reservoirs (among oth- ture carries examples of instances when expe- ers, Haffner et al., 1980;Reynolds, 1980a;Trimbee riences differed from expectation. For instance, and Harris, 1983;Viner and Kemp, 1983;Ashton, thefact that an episode of summer storms and 1985;Gaedke and Sommer, 1986;Olrik, 1994). floods failed to break the dominance of Aphani- Reynolds’ (1980a)usageoftheterms ‘shift’ zomenon in the plankton of a small Danish lake, and ‘reversion’ to refer, respectively, to the dis- while earlier, relatively trivial, weather events ruption of the succession by cooling/mixing had triggered upheavals of species composition events associated with passing weather systems, wasquite clearly contrary to the anticipation and to its subsequent recapitulation, now seems of Jacobsen and Simonsen (1993). Other authors too mechanistic (too Clementsian? cf. p. 351); have noted that the resistance of communities abandonment of these terms was recommended to disruption by external forcing is acquired pro- (Reynolds, 1997a). Nevertheless, the experimen- gressively with increased successional complexity tal manipulations of succession and disturbance (Eloranta, 1993; Moustaka-Gouni, 1993;seealso imposed by Reynolds et al.(1983b, 1984) attest to Barbiero et al., 1999). Sommer (1993) has shown the importance of steady physical conditions in that in neighbouring lakes of similar chemistry allowing autogenic processes to structure com- but differing morphometry, disturbance events munities and to dominate assembly processes. were more extensive and effective in increasing Equally, they show how variations in the physical diversity in the deeper example. The responses of conditions may terminate one autogenic phase theplankton differed among three small lakes of and initiate the next. contrasted trophic state and compared by Holz- The physiological responses of the phyto- mann (1993), being weakest in the most olig- plankton to an altered physical environment are otrophic of them. In reviewing each of these con- immediate but take several hours or more to feed tributions, Reynolds et al.(1993b) concluded that through to altered population recruitment rates. there is no consistent or predictable relationship Accelerated rates of community change (σ s)and between diversity and external physical forcing. higher instantaneous diversity indices (H , Hs) For terrestrial ecologists, the development of a are evident within days. From the cited Blelham consistent theory of disturbance has been just as enclosure studies, Reynolds (1988c)deduced that, troublesome (e.g. Wilkinson, 1999). There is little depending upon the relative dominance of the difficulty in understanding the intervention of disfavoured species, σ s reaches a maximum after catastrophes, from fires and storms to volcanic two to four generations of the favoured species eruptions and lava flows, in being able to arrest, have been recruited to the plankton. The diver- not to say to obliterate, the autopoetic develop- sity index (Hs)followsclosely. In real time, this ment of terrestrial vegetation and the reopen- might be equivalent to 4–16 days after the stim- ing of the land surface to colonising propagules. ulus is applied. This deduction agreed substan- Neither is there a problem in recognising that tially with the findings of Trimbee and Harris stochastic, smaller-scale forcings create just the (1983)andGaedke and Sommer (1986). There is generally fluctuating environment that prevents now general agreement that diversity is highest theextinction of opportunist strategists by persis- early in the disturbance response, around the sec- tent resource gleaners (see, for instance, Pickett et ond to third generation, or within 5–15 days of al., 1989). Indeed, the simultaneous existence of the impositionofthestimulus (Reynolds et al., sources of invasive species actually necessitates a 1993b). continuity of disturbances and a continuum of patches in differing stages of successional matu- IDH and diversity ration among which invasive species may migrate Despite the satisfyingly simple elegance of (Reynolds, 2001a). It is also self-evident that, were the concept of disturbance-induced community this not the case, opportunism (r-selection) would restructuring and of disturbance-impeded suc- cease to have any viability as an adaptive survival cessional progression (the searching critique of strategy. This view of patch dynamics is explicit ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 375 in Connell’s (1978)hypothesis and is implicit in only must it be a signal that can feed through Hutchinson’s (1961)suggestedexplanation of the to species-specific growth rates but the potential plankton paradox, when he referred to ‘contem- respondents have to be moved from their contemporaneous disequilibrium’. A further corollary is poraneous limitation. Put simply, if the phyto- that, as all species have evolved to contend with plankton is experiencing growth-rate limitation disturbed environments, they are, in a sense, through an effective lack of (say) iron or phospho- matched to recurrence of perturbating events rus, it is difficult to imagine how exposure to 1 to (Paine et al., 1998). Thus, we may note again that 2daysofstrong winds and a simultaneous deep- dispersal constraints are as important to com- ening of the surface mixed layer from <3to∼7 munity assembly as is the inevitability of self- mwill overcome that. The forcing does not dis- organisation and the stochasticity of external disturb the status quo ante.Yetthiswasthe extent of turbances. forcing applied to Crose Mere needed to disturb The problems experienced by terrestrial ecol- thesummer succession, to stimulate a significant ogists relate mainly to inconsistencies of pattern, bloom of diatoms and to raise the planktic diver- especially relating to the intensity and frequency sity (Reynolds, 1976a) (and see p. 373). of disturbances considered to be effective in influ- The experience of this observation from the encing diversity, and which of these might be field should always prompt the question: is the the morecritical (Romme et al., 1998;Turner et potential of the forcing sufficient to overcome al., 1998). There are difficulties in the scaling of theexisting structure? At the present time, this models based on field observations and differ- is not easy to answer from any quantified standing inputs can raise or suppress the response of point, without some common units. The poten- diversity to disturbance (Huston, 1999; Mackey tial of comparing external mechanical forcing and Currie, 2000;Hastwell and Huston, (2001). with the current cushion of exergy flux (in In another modelling approach, Kondoh (2001) MJ m−2 d−1) has been explored theoretically in purported to show the important interaction Reynolds (1997b). An accumulating phytoplank- between system productivity and distubance in tonwas challenged by wind-mixing events of influencing the competitive outcome of multi- known kinetic energy. From the starting assump- species dynamics on species richness. In essence, tions about temperature (set at 20 ◦C), the possi- arelationship between diversity and disturbance ble income of solar energy (≤26.7 MJ m−2 d−1; is confirmed as being unimodal but the pro- say, 12.6 mJ m−2 d−1 harvestable energy), and ductivity level that maximises diversity itself the mechanical energy required to disperse this increases with increasing disturbance. uniformly through 1 m (65 J m−2 d−1;equiva- In a way, this seems to match the deduc- lent to a wind of 3.4 m s−1), wind forcing was tions in respect to lake productivity (Holzmann, increased selectively with a view to balancing the 1993;Reynoldset al., 1993b): that productive or incoming flux. By itself, mixing energy offers lit- nutrient-rich systems are more susceptible to dis- tle challenge to the harvestable energy flux: even turbance than nutrient-poor ones. This, indeed, with a tenfold increase in wind speed (34 m s−1), would make a satisfying conclusion. However, it thekinetic energy flux is still only 6.5 kJ m−2 offers no real explanation for its mechanisms in d−1.However, the simultaneous deepening of the nature and it also perpetuates one of the most mixed layer dilutes greatly the harvestable energy persistent shortcomings in applications of the available to entrained phytoplankters (see p. 138). IDH. Taking the second point first, every observ- Even a doubling of wind speed is sufficient to able disturbance is a response reaction, an out- increase the depth of mixing of the modelled come of internal dynamics of the species inoc- water by the cube, that is, to 8 m. Using various ula present. It is to be differentiated from the interpolations of existing phytoplankton biomass forcing applied, which may, or may not, evoke a (1–100 mg chla m−2), its assumed light absorp- 2 −1 response at the level of population recruitment. tion, εa = 0.01 m (mg chla) ,andoftheback- −1 Only then is a disturbance precipitated. This is ground extinction of the water (εw = 0.2 m ), where the intensity of forcing is critical – not thelevels of energy harvestable by phytoplankton 376 COMMUNITY ASSEMBLY IN THE PLANKTON

Figure 7.20 Energy exchanges and exergy accumulation Figure 7.21 Representation, against the under a varying capacity. The sigmoid line traces the potential energy-accumulation model (Fig. 7.11)ofthe responses of accumulation (cf. Fig. 5.20, 7.12e) but this experiences biomass to capacity oscillations, including readjustment (a setbacks every time that the sustainable biomass exceeds the disturbance) when the accumulated mass is left unsustainable. capacity of the oscillating energy income. On each occasion, Redrawn with permission from Reynolds (2002b). there has to be an adjustment (losses of structure, mass and exergy) which is manifest as system disturbance. So long as energy or resources continue to fluctuate, ecosystems go on alternating between expansion into available capacity and by wind mixing, variability is such that it is readjusting to contraction Redrawn with permission from indeed possible that the energy that is actually Reynolds (1997a). harvestable may, on occasions fall below the minimum maintenance requirement of the accumulated phytoplankton biomass. Against the plot in could be reduced to <6MJm−2 d−1. When the Fig. 7.11,this is equivalent to saying there is insuf- exclusive effect of increased mixing due to the ficient harvestable energy to maintain a positive doubling of mechanical stress is compounded by exergy flux. In short, the system is unsustainable. changes day length, cloud cover and lowered radi- So long as the external condition persists, the ation intensity, the harvestable energy is quite requirement to restructure (lose biomass, place liable to reduction to low values (often <2MJ biomass in a lower energy resting state; switch m−2 d−1). to more light-efficient species) becomes likely to Thus, mechanical disturbance arguably car- invoke a response that might be perceived as a ries entropic penalties of a magnitude sufficient disturbance. The energetic representation is used to disturb community development in the plank- as the basis of Fig. 7.21,inwhich the variabil- ton. Without more empirical data, however, it ity in the potentially sustainable biomass (against remains a conjecture. Nevertheless, the conjec- variable energy income and mechanical dilution) ture yields a further, simple conceptual model is tracked as a function of the actual biomass. of the link between forcing and the manifes- We can readily appreciate that forcing variabil- tation of diversity-raising disturbances. In Fig. ity absorbed within the harvesting capacity and 7.20,ahypothetical plot tracks through time the leaving a positive exergy flux is fully sustainable biomass potential of an ascendent phytoplank- and does not constitute a disturbance. Should ton (and, hence, of its finite energetic require- the forcing result in an energy income that is ments of maintenance) and the simultaneous insufficient to balance maintenance, there is no supportive capacity of the harvestable energy exergy buffer left. Eventual reaction is inevitable, flux. With daily fluctuations in the incoming although the scale of disturbance may yet depend solar flux and of daily fluctuations in its dilution upon the scale of exergy shortfall (intensity), its ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 377

Figure 7.22 Arithmetical means of (a) species number, (b) equitability and (c) Shannon diversity in periodic phytoplankton showing disturbance responses as a function of their frequencies. Most of the data refer to events in Balaton (B) in the summers of 1976–78, 1980 and 1982, before (B82bb) and during (B82b) the enduring Cylindrospermopsis bloom that year. Other points are for (N) Neusiedlersee, an experimental pond (e) and its control (c). Note that all three plots peak at disturbance frequencies of 3–7 days. Original data of Padis´ak (1993) and redrawn with permission from Reynolds (1997a).

duration and the physiological resistance of the judgement. The evidence from Padisak’s´ (1993) accumulated biomass to withstand the energetic collected sequences of phytoplankton in various disequilibrium. The track in Fig. 7.21 shows the Hungarian lakes (see Fig. 7.22)showsspecies rich- necessary scaling down of biomass costs and the ness, equitability and Shannon diversity each to reversion to an earlier ascendent stage. Inciden- rise steeply from daily disturbances up to separa- tally, it also implies a low incidence of distur- tion intervals of 3–7 days. Thereafter, each index bance at low biomass (as does Fig. 7.21), including decayed gradually back to low average levels at those instances of severe nutrient constraints (cf. infrequent disturbances (separated by >30 days). Fig. 7.15b). The other valid way of expressing frequency, as With a clearer picture of what constitutes a anumber of disturbances per year, was used by disturbance, we may now return to the central Elliott et al.(2001a)asabasis for applying simu- issue of diversity being a function of the fre- lated forcing events on periodic sequences mod- quency of disturbance. From Connell himself to elled using PROTECH (see Section 5.5.5). Exter- many subsequent authors elaborating on the IDH nal forcing to a controlled physical environment (e.g. Wilkinson, 1999), the relationship between wasdevised (actually an instantaneous, complete diversity and frequency of disturbance is repre- mixing of a hitherto stratiﬁed 15-m water col- sented as a smooth parabola, generally referred umn, mixed to only 5 m) while all other vari- to as ‘the humpback curve’. It successfully con- ables (day length, incident radiation, tempera- veys the idea of low diversity occurring at zero ture and saturating nutrient availability) were and at very high frequencies of disturbance and held constant. Grazing of algae was excluded. of higher diversities at intermediate frequencies Eight species of phytoplankton having contrasted (p. 373). However, there is no basis for assum- life forms and survival adaptations were seeded ing a continuous relationship with frequency, on day 1 and their dynamic changes were then even if scaled in terms of respondent gener- simulated over a period of 1 year. Model runs ations. Neither do most terrestrial sources of were subjected to applied forcings, with vary- data provide much information to form any real ing frequency and duration, and the population 378 COMMUNITY ASSEMBLY IN THE PLANKTON

Chlorella): it achieved immediate dominance and thevirtual exclusion of all rivals (i.e. low diversity) within 50 days. Inserting two or three 7- day forcings during the year (Fig. 7.23a) produced theequivalent number of clear disturbances, in which a brief maximum of species B (having the relevant properties of R-strategist Asteri- onella)wassupported. On reversion to the ambient state, species A (‘Chlorella’) duly reasserted its dominance and species B (‘Asterionella’) dropped back. Increasing the forcing frequency to five per year (Fig. 7.23b) has the effect of maintaining amorevaried plankton, with ‘Asterionella’ alternating in dominance with ‘Chlorella’andother species being represented more strongly. At frequencies of 25–30 forcings per year, the forced and alternating quiescent periods become quite similar in length (Fig. 7.23c) and are sufficient to allow ‘Asterionella’todominate ‘Chlorella’throughout while other species remain in contention. Over a broad range of disturbance frequencies (6–30 a−1), the average Shannon diversity (H)of thesimulated eight-species assemblage is about 1.8ofapossible 3.0 bits mm−3 (evenness ∼0.6). Increasing the frequency yet further, a sharp alteration in behaviour was found to occur between 31 and 32 a−1 (i.e. quiescent periods are each <5d(Fig.7.23d). The system changed to persistent dominance by a third species, C (having the relevant properties of R-strategist but more K-selected Planktothrix agardhii), eventually to the exclusion of all the other species. Its pre-eminence was enhanced at still higher frequencies up to the point of continuous mixing Figure 7.23 PROTECH-simulated changes in the to 15 m. populations of phytoplankton species to a standard physical Changing the forcing to 5- or to 3-day peri- forcings (complete and instantaneous vertical mixing of an otherwise stratified 15-m water column for 7 days) applied at ods produced analogous sequences of results, various frequencies. Periods of imposed forcing are shown by although correspondingly higher frequencies the short horizontal bars. The ‘species’ correspond to were needed to avoid the replacement of ‘Plankto- Chlorella (A), Plagioselmis (B), Asterionella (C) and Planktothrix thrix’ during the ‘intermediate quiescence’. The (D). Note the precipitous change to Planktothrix dominance latter term had been introduced previously by when 32 rather than 31 disturbances are applied. Redrawn Chorus and Schlag (1993)inthecontext of inter- with permission from Elliott et al.(2001a). ruptions (disturbances) to the success of Plankto- thrix in rich, turbid lakes that are normally sub- responses were also monitored for 1 year. Under ject to persistent mixing. the ambient, unforced conditions, the commu- In all the series, surpassing the critical scale nity became quickly overwhelmed by the fastest of forcing frequency secured an abrupt decline growing life form (speciesAinFig.7.23, actually in Shannon diversity (to H < 0.8). Plotting diver- having the relevant properties of a C-strategist sity as a function of forcing frequency (Fig. 7.24a) ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 379

Figure 7.25 Species diversity plotted as a function of the frequency of externally forced disturbances, as the smooth ‘humpback’ usually supposed in many previous considerations of the IDH, and as the ‘cliff-shaped curve’ revealed by PROTECH modelling. Redrawn with permission from Reynolds and Elliott (2002).

Figure 7.24 Annual mean Shannon diversity of PROTECH-simulated phytoplankton assemblages, in terms of contributing to high diversity but several. As (a) frequency of 7-day forcing events, and of (b) the time Hutchinson himself understood well, the para- intervals separating forcing events of 3-, 5- and 7-day duration. dox lies wholly in the initial assumptions. Except Redrawn with permission from Reynolds and Elliott (2002). under very well mixed conditions in a small (<10 km2) and relatively shallow lake basin, there is no single, homogeneous, isotropic environ- shows the expected low diversity at both very low ment. Even there, dynamic water movements are and very high frequencies of alternation. Plotted so variable that there is almost no opportunity in terms of the interval between forcing events forany kind of physical steady state to estab- (Fig. 7.24b), diversity first increases steeply as qui- lish. There is a virtual simultaneity of adjacent escent periods lengthen, achieves a maximum in patches, each experiencing differing conditions, therange 10–50 days and then falls away with yet which will themselves soon alter again, per- ongoing physical stability. The modelling plainly haps critically and perhaps in less time than it confirms the prejudices about intermediate dis- takes an alga to complete a generation. Only in turbance and its critical times. What is also of the case of the most severe and ongoing depriva- general interest is the deduction of Elliott et tion of a particular nutrient, or of the harvestable al.(2001a)that the relationship of diversity to energy input sufficient to satisfy the mainte- forcing frequency is not the smooth humpback nance requirements of most producer biomass is curve that is popularly represented but one with theeffect of this physical environmental variabil- amore cliff-like cut-off at critically high distur- ity overridden. Moreover, because algae are dif- bance frequencies (Fig. 7.25). ferentiated by their adaptations to function and to continue to grow in differing combinations of Explaining the plankton paradox: where does various environmental constraints, they show dif- the diversity come from? fering dynamic responses and response times to Over 40 years of research since Hutchinson (1961) environmental variability, sufficient indeed for posed the paradox of the phytoplankton have habitats to maintain several species in simulta- succeeded in revealing many more verifications neous and alternating contention. And, because of the diversity of natural phytoplankton assem- local species exclusion, whether as a direct result blages, whereas its explanations have emerged of unsuitable prevailing conditions or through only gradually. For there is not one mechanism one species being outperformed by others when 380 COMMUNITY ASSEMBLY IN THE PLANKTON

the prevailing conditions are suitable, requires Though strongly apparent in the phytoplank- alapseof time equivalent to several algal gen- ton, the dynamic nature of ecological diver- erations, local extinction is also correspondingly sity with respect to habitats or global popula- rare. Finally (and perhaps crucially), most locations had not always be appreciated or empha- tions preserve an ecological memory in the infor- sised by ecologists generally. More recently, ter- mation banks represented by the overall species restrial ecologists have embraced the importance richness. Like the handful of conspicuous domi- of the larger-scale processes, within the separate nants, their numbers also wax and wane through subdiscipline ‘macroecology’ (Brown and Mau- time; local diversity is enriched by the poten- rer, 1989). Of particular interest are the rela- tial of what is usually the majority of rare local tionships among what is referred to as the α- species to be abletoappearinoneoftheniches diversity (that recruited locally and equivalent to that events conspire to make available. thephytoplankton species list of a single, hydro- It is also evident that, in the event of relatively logically isolated small lake) and to the richness more extreme environmental forcing events, of the regional pool, whence local exclusions resulting in larger-scale, catastrophic reductions might potentially be replenished (γ-diversity; say in biomass (e.g. flushing, storm disruption), the that of the same geographical zone, or part of recovery of a functional phytoplankton (albeit the ocean). Of considerable concern to the con- ‘disturbed’ as defined herein) is fully possible. servation of terrestrial biodiversity, especially of In addition to a certain resistance of late suc- macrovegetation and vertebrate fauna, is the risk cessional stages to destruction by mixing events to both local and regional diversity of habitat (that is, species-specific biomass is robust in with- fragmentation into smaller units (e.g. Lawton, standing – and recovering from – conditions 2000). Just as macroecological systems are sepa- that, for a time, are arguably unable to satisfy rable on the basis of their habitat (β-) diversity, its maintenance needs), the species composition they tootend either to Type-I behaviour, in which is also demonstrably resilient to forcingevents. local species richness is fluid and proportional By this, we mean that the respondent commu- to regional richness or to Type-II local richness nity is based upon new growth of a similar being constrained above a certain proportion of selection of the same species that were present theregional richness. before the destructive forcing, so that the post- Being mutually separated, most freshwater disturbance species composition may come to systems have the character of isolated islands resemble the pre-disturbance one, albeit in new and, so, are expected to conform to the con- proportions. This is not surprising in itself, being straints of island biogeography (MacArthur and attributable in many instances to the recruit- Wilson, 1967). Moreover, the obvious connec- ment of inocula biased by the survivor vegeta- tivities within predominantly linear structures tive biomass or by the germination of conspe- are essentially gravitational. Thus, the broad- cific local propagules (the ‘seed bank’) formed est recruitment pathways for freshwater biota in previous extant phases (Reynolds, 2002c). How- are provided by downstream transport, whereas ever, the further source of specific biomass that mobility between catchments relates to organis- is important to re-establishing pelagic assem- mic size and efficiency of dispersal. As is we have blages is the arrival of species-specific inocula seen (Eq. 7.3), microalgae, like bacteria and micro- from adjacent and more distant patches, exploit- zooplankton, move very freely between catching effectively the channels of dispersion iden- ments and are highly cosmopolitan among suit- tified above (see p. 353). Post-disturbance phyto- able habitats over most of the world. Given plankton assemblages retain an ongoing capacity that detailed lists of species of phytoplankton to yield just those compositional surprises that recorded in individual well-studied sites may make the study of phytoplankton ecology so fas- comprise between 100 and 450 species (see p. 354) cinating. This is also the main mechanism of the and supposing that the regional species richness apparently cosmopolitan and pandemic distribu- lies within the order of magnitude 500–5000, tions of most phytoplankton. then habitat suitability probably distinguishes ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 381 the100 or so commonly encountered species ecology permit the application of observations in the local assemblage. Of the latter, fewer to theresolution of outstanding theories, predic- than eight species account for most of the local tions and models derived in ecological investiga- biomass at any one time. These also account for tions of other systems. most of the measured local (α-) diversity. The implied generality of these relationships 7.3.4 Stability and fidelity in phytoplankton is perhaps indicative of the intuitive Type-I phy- communities toplankton diversity, in which local species rich- After the preceding discussion of variability and ness represents a sub-set of the regional pool that disequilibrium in the plankton and the great has somehow satisfied the twin constraints of distance away from steady state at which most having ‘passed the filters’ (Keddy, 1992)ofdis- planktic communities are poised, any explo- persal and habitat suitability. Beyond that, the ration on the topic of their stability may seem actual mix of species and the relative propor- vaguely fatuous. On the other hand, many exam- tions in which they appear seems stochastic and ples of patterns in species composition and tem- unpredictable (Rojo et al., 2000). On the other poral change in phytoplankton assemblages in hand, planktic assemblages frequently support a Section 7.2,bothinmarineandfreshwater sys- high information content (H 3–5 bits mm−3). tems, were shown to apply widely among similar This might equally imply that species interac- types of water body. Many examples of broadly tions contributed only weakly to a Type-I diver- repeatable annual sequences of species abun- sity. dance were cited. They evidently carry a rela- To be set against this are the many cases tively low coefficient of interannual variation of low-diversity, near-unialgal structures wherein (CV), calculable as the ratio of variance to mean similar species or life forms are consistently biomass. Moreover, taken at the widest geograph- and predictably selected in geographically quite ical scales, individual species are typically either remote locations: we think of the common domi- common or generally rather rare. nance of Microcystis or Planktothrix or Ceratium. The Given a predictable level of constancy about organisation of species assemblages around per- therelative global abundances of phytoplankton sistent gradients of nutrients, light and redox is species, this high fidelity of cyclical behaviour similar from the equator to the poles (Reynolds, is symptomatic of the kind of long-term stabil- 1988c). Regional variations in the participating ity that was once supposed to characterise all species are evident but the functional specialisms developed ecosystems. It used to be believed, of the dominants are wholly analogous. The uni- forexample, that the perceived stability of for- formly low α-diversity that is achieved is indepen- est ecosystems was a consequence of their com- dent of the regional richness and, thus, is quite plexity (Elton, 1958;Hutchinson, 1959,quoted unmistakably indicative of Type-II behaviour. by Southwood, 1996) and food-web interactions Poised between Type-I and Type-II mecha- (Noy-Meir, 1975). These assumptions about sys- nisms, the overall deduction about biodiversity temstability are now seriously questioned (May, in the plankton is that it is maintained through 1973;Lawton,2000). On theoretical grounds, May the combination of variable forces – environ- (1973) showed that, far from increasing stability, mental oscillations, disturbances and recovery complex interactive linkages increase the oppor- from catastrophic setbacks – backed by a pow- tunities of chaotic behaviour and, thus, should erful dispersive mobility of organisms among decrease stability. Appropriate modelling of phy- spatio-temporal patches. The same mechanisms toplankton species composition concurs with this resist the extinction of the majority of rarer sub- argument (Huisman and Weissing, 2001;Huis- dominant species. The conclusion concurs with man et al., 2001). Yet it is perfectly evident and the theoretical predictions of Huston (1979)and generally accepted that complex ecosystems con- the models of Levin (2000), both based on the form to theideal of low-CV stability, oscillat- behaviour detected among terrestrial ecosystems. ing about one or another characteristic stable Once again, the small timescales of plankton condition. May (1977)memorably analogised the 382 COMMUNITY ASSEMBLY IN THE PLANKTON

behaviour to a ball in a depression on an uneven cycle has remained the prerogative of just one or surface, gently rocked by external forcing. The two species. Any of the others of the same func- movements of the ball are focused on a stable tional group is presumably able to fulfil the role location position; however, it remains liable to of the dominant, should the incumbent species amore violent, chaotic event that may dislodge underperform for any reason. Significant inter- the system, perhaps irreversibly, into an adjacent annual differences in species composition are hollow, representing an alternative stable state. prompted by periodic habitat variations, such as As May (1973) had deduced, this means that temperature structure and wind-mixing, forced ecological stability depends upon the stability by El Niño activity (Karl, 1999, 2002). of the physical habitat and that the determin- The observation is relevant to the question, ing interactive linkages are not at all random raised at the outset of Section 7.3.3,about the but are a selected set. Viewed from the stand- importance of high diversity to the function- point of phytoplankton ecology, the first of these ing of complex ecosystems. The early debate lay conditions is explicit (see p. 317). The notion between two extremes. The ‘rivet theory’ (Ehrlich that, where physical constraints allow, increas- and Ehrlich, 1981)supposed that because every ing species richness helps to stabilise aggregate species plays a part in the ecosystem, like the riv- community responses is also well established. ets in an aircraft, each one that is lost impairs Cottingham et al.(2001)recentlyreviewedsev- performance, eventually to a point where it can eral studies that measured species richness and no longer fly. At the other end of the spectrum, variability. They concluded that the evidence it was recognised that, provided each of its essen- fortight coupling of these properties is not as tial DEU functions is fulfilled (see p. 351), it is per- unequivocal as they had supposed previously. fectly possible for species-poor systems to func- Methodological difficulties of sampling and scal- tion adequately. Thus, most species tend to be ing in the original studies may have contributed functionally redundant within their habitats (B. to their findings. However, theywereabletover- H. Walker, 1992;LawtonandBrown,1993). Nowa- ify that, while fluctuations in the populations of days, a more consensual understanding pervades, individual species vary independently of species that the contributions of individual species to richness, or may actually increase with greater given systems are generally unequal. Some, the species richness, the total biomass frequently so-called ‘keystone species’ (Paine, 1980), will ful- aggregates around a stable level. In other words, fil the role of major repositories of organic car- community variability decreases with increased bon or they may play a disproportionately bigger species richness, despite possibly increased vari- role in energy transfer. Some species may play ability in the contributions of individual species. astructural role in the sense that they modify This concurs with analyses of zooplankton data (or ‘engineer’: Jones et al., 1994)theenvironment subject to planktivory. Ives et al.(1999,(2002)pro- to the benefit of other exploiters (forest trees posed that, subject to the condition of low envi- and the microhabitats and trophic niches they ronmental variability, increasing the number of furnish come immediately to mind). This still species in a community decreases the coefficient leaves a large number of species that are func- of variation of the summed species concentra- tionally superfluous or, at best, mere ecosystem tions (aggregate biomass). passengers. With reference to the interannual variabil- The results of some ingenious field experi- ity of the supposedly most stable phytoplankton ments, involving terrestrial herb communities, structures (those of the North Pacific Subtropical help us to resolve a general view of the func- Gyre; see p. 304), we are now able to appreciate tional role of species richness and local species the disproportion of the long-term species rich- biodiversity. Wilsey and Potvin (2000)reduced ness. Just 21 of the 245 species recorded over 12 the numbers of dominant plants from old- years byVenrick (1990)havetogether contributed field communities, though without reducing the 90% of the aggregate biomass, while the long- overall species richness. They found that aggre- term dominance of any given stage of the annual gate biomass increased in proportion to evenness, ASSEMBLY PROCESSES IN THE PHYTOPLANKTON 383 independently of which species had previously network linkages (for further discussion, see been dominant. In the experiments of Wardle Loreau et al., 2001). et al.(1999), plants of the most aggressive of the grass species present, Lolium perenne,were 7.3.5 Structure and dynamics of removed altogether from a perennial meadow phytoplankton community assembly in New Zealand. There followed an increase in In order to weave together the multiplicity of biomass of the species remaining, while rich- threads gathered in this exploration of the pro- ness was increased by germlings of invading cesses governing the assembly of phytoplankton species. For a time, at least, a broadly similar communities, some conclusions now need to be function was maintained in the grassland. When aligned. they removed all the plants, of course, there were immediate repercussions in other ecosys- (1) Development of phytoplankton can take tem components, most notably among the nema- place, subject to the assembly rules proposed tode consumers and their predators. Wardle et in Table 7.8,withintheconstraints of the al.(1999)deduced that the deliberate exclusion environmental carrying capacity. The latter of the dominating (high-exergy) species promotes may be set by the nutrient resources avail- the nextfittestofthe species available within the able or the daily harvestable light income, as same functional group to assume the same func- regulated under water through the interac- tional role in the modified ecosystem. tion of mixed depth and the vertical coef- Iamnotawareofacomparable experiment ficient of light extinction. While capacity involving phytoplankton, save as an alternative remains unfilled, there can be recruitment of to macrophytes and periphyton, as considered biomass through growth (Rule 1, Table 7.8). At in Chapter 8.However,thePROTECH model (see such times, there need be no competition for Section 5.5.5)iseminently suited to the simula- thelight and resources available. The oppor- tion of this kind of manipulation. Elliott et al. tunity is exploitable by all species present (1999a, 2001b) compared the rate of development, and whose minimal requirements are satis- the maximum biomass attained and the diversity fied. Of these, the species with the highest of phytoplankton communities serially stripped exergy and fastest sustainable net rates of of the best-performing species. In each instance, increase growth should benefit most (Rule 2, attainment of capacity was noticeably delayed Table 7.8). Spare capacity is thus beneficial but evenness among the remaining species was to net productivity (Pn/B)andtoincreased increased. species richness. Equally, if biomass is equal The essential contribution of otherwise appar- to,orexceeds, the current capacity, recruit- ently functional redundant species to commu- ment is weak. Survivorship is influenced in nity and ecosystem function seems to lie in their favour of species having greater affinity for potential to assume primacy when the perfor- the capacity-limiting factor and/or superior mance of the existing dominants is impaired adaptations to withstand the adverse con- forany reason, either internal (due to interac- ditions. Competition for the limiting factor tion with other species) or external (imposed works against species richness but competi- changes in filtration by environmental variables). tive exclusion is slow if the development of Aresilient ecosystem is characterised by a net- even the superior contenders is constrained. work of energy-flow linkages, whose individ- (2) The locally available species (richness) ual connections may strengthen or weaken in depends, in part, upon the local ‘seed bank’ response to fluctuations elsewhere. Interventions of propagules (Rule 3, Table 7.8). However, affecting the performance of key species and, thehigh rates of transmissibility among in consequence, those to which they are troph- phytoplankton (low z value in Eq. 7.3)make ically linked, are compensated to a great extent for abundant immigration opportunities by the enhanced performances of hitherto sub- and high rates of invasion or reinvasion dominant species and the strengthening of their from remote sites. Relative importance of 384 COMMUNITY ASSEMBLY IN THE PLANKTON

local or invasive recruitment varies among through succession. Given sufficient time and phytoplankton, mainly with relative size and with constant probabilities, the possible cli- r–K selectivity. mactic endpoints of succession are few in (3) Species richness may vary through the number and predictable for the region, its cli- dynamics of local recruitment and local mate, catchment and limnological character- extinction. There is evidence of long sys- istics. tem‘memories’, with vestigial populations re- (6) Species diversity in accumulating communi- enacting the seasonal cycles of growth and ties is likely to be relatively higher than in attrition evident in previous days of abun- maturing successions. Species diversity is also dance. Although some prominent species greater where there is structural diversity of return to dominance year after year for long the habitat (such as in a stably stratified lake). periods, there may be a slow change in Species richness in accumulating communi- the species representation and richness (Ven- ties is not generally related to productivity rick, 1990). This turnover may be slow on or trophic state. According to Dodson et al. interannual scales but it may vary over cen- (2000), species richness shows a flattish but turies (a fact exploited by palaeolimnologists unimodal relation to area-specific primary reconstructing habitat changes at the millen- production, peaking in the range 30–300 C nial and greater scales: Smol, 1992;Smolet m−2 a−1 (which range covers moderately olig- al., 2001;O’Sullivan, 2003). Species richness otrophic to moderately eutrophic systems). and/or dominance is liable to abrupt alter- (7) Autogenic maturation of communities is ation in the wake of critical environmental exposed to disruption by allogenic physical or change (eutrophication, acidification). chemical forcing. This the communities may (4) Planktic systems are continuously liable to survive (resistance) or recover from (resilience) invasion by species that are not already or the community is restructured through a present or abundant. Such invaders do not forced replacement of biomass and dominant become prominent unless their adaptations species by others more suited to the new con- are better suited to the local environment ditions. The response is disturbance. Commu- than are those of existing species (a recent nity disturbances imposed at a frequency of example is the spread of Cylindrospermopsis two to four algal generation times maintain raciborskii,ascatalogued by Padisak´ (1997)) thehighest mix of available species and thus and achieve a higher exergy, with faster net high levels of diversity. By virtue of the near recruitment rates, than existing dominants. prevention of competitive exclusion, distur- (5) While habitat variability remains slight, com- bances of this frequency constitute a major munities develop towards a steady state, gen- driver of continuing high diversity and rich- erally dominated by one of a small selec- ness levels (p. 377). However, the mobility of tion of suitably adapted species (Rules 4–7, species and their ability to re-establish from Table 7.8). This autogenic development has other locations may be critical to this process. long been known (as succession); the properties The mechanisms resist the extinction of the of maturing successions are also well known majority of rarer subdominant species. (Table 7.7). The long-standing desire to explain (8) Annually recurrent cycles of seasonal algal successional sequences of species composi- dominance suggest a high level of inter- tion must defer to the evidence that there annual constancy in pelagic habitats. Simi- is no continuous sequence of species, rather lar environmental conditions, roughly reca- aprobability of certain outcomes relating to pitulated each year, renew similar filtration the fitness and adaptations of the species pool effects upon a species pool, which in conse- available (Rules 8 and 9, Table 7.8). Succes- quence becomes biassed in favour of species sion is a cycle of probabilities of replacement that have grown well in recent seasons. of dominant species. Diversity (though not The development of ‘commonness’ among necessarily overall species richness) declines regional species pools also influences the SUMMARY 385

similarity of seasonal pattern among region- thephysical environment in regulating both ally similar types of aquatic systems, consid- the abundance and composition of the phyto- ered in Sections 7.2.1 and 7.2.3. plankton. These provide the axes of the generalised habitat templates, developed by Smayda and Reynolds (2001), to which the main assem- 7.4 Summary blages of marine phytoplankton are consistently aligned. Patterns in the abundance and composition of Species assemblage patterns in lakes respond natural phytoplankton assemblages in the sea to analogous drivers, with some strong coher- and in lakes are sought in this chapter. In ences among major floristic components with the sea, characteristic floristic associations with regional climates, lake morphometries and the extent, longevity and supportive capacity catchment-derived nutrient loads. Among the of the water in the major oceanic circulations world’s largest lakes, pelagic environments are demonstrated. Environmental distinctions resemble the open ocean in the deficiency of from adjacent shelf and coastal areas and from nutrients and the importance of mixing, and localised upwellings, coastal currents and fronts they show a similar community organisation are shown frequently to offer greater carrying based upon picophytoplankton and microbial capacities, higher levels of biomass and different processing of fixed carbon. However, at all lat- planktic associations. itudes, density stratification (including under The tropical gyres of the Pacific, Indian ice) is a prerequisite of significant communal and Atlantic Oceans are profoundly oligotrophic, growth and assembly. Among moderate to small nutrient deficient and permanently stratified lakes, phytoplankton abundance and composi- beyond a depth of ∼200 m. Phytoplanktic tion is demonstrably constrained by nutrient biomass is severely constrained, often <20 mg supplies and by the underwater light climate. chla m−2.Forlongperiods, the dominant Both are instrumental in setting limits on the primary producers are picoplanktic Cyanobac- carrying capacity and in influencing the adap- teria, the fixed carbon being cycled mostly tive requirements of the favoured phytoplank- through the microbial food web. Changes in tonspecies. Seasonal periodicities, broadly mov- near-surface stratification, wrought by weather ing from (w-selected) diatom abundance in mixed events or longer-term climatic fluctuations, stim- columns to colonist (r-selected) nanoplankters ulate episodes of recruitment of nitrogen-fixing and then to increasingly specialist (K-selected) cyanobacteria (Trichodesmium)anddiatoms (Hemi- microplankters, reveal consistent patterns. How- aulus)ordeep-migrating dinoflagellates. ever, differences in maximum biomass and in In contrast, primary production in the high dominant functional types usually reflect differ- latitudes is constrained by strong seasonal fluc- ences in resource richness. Phosphorus-deficient tuations in light income, temperature and phys- oligotrophic lakes support low biomass com- ical mixing. A small number of diatom species prising distinctive diatoms (Cyclotella bodanica are overwhelmingly dominant, but dinoflagel- group, Urosolenia), desmids (Staurodesmus, Cosmar- lates and the haptophyte Phaeocystis are some- ium), chrysophytes (Dinobryon) and dinoflagel- times abundant. In boreal and mid-latitudinal lates (Peridinium). Picophytoplankton may make waters, diatom dominance alternates seasonally up a substantial proportion of the biomass. with nanoplankter and dinoflagellate abundance. In eutrophic (P-rich) lakes, other diatoms, nos- In shelf and coastal waters, supportive capacity is tocalean Cyanobacteria and self-regulating Cer- generally muchhigher than in the open ocean atium species may have eventually to be able but the more abundant phytoplankton shows to contend with shortages in the rates of strong seasonal periodicity. supply of carbon and nitrogen, while high Margalef’s (1958, 1963, 1967, 1978)deep turbidity may force light constraints favour- insight has contributed greatly to a broad under- ing filamentous cyanobacteria, diatoms and standing of the separate roles of nutrients and xanthophytes. 386 COMMUNITY ASSEMBLY IN THE PLANKTON

These behaviours help to explain the fit of ultimately depend upon their specific evolution- groups of species (trait-selected functional types) ary attributes and adaptive traits and upon their to analogous templates defined by axes scaled appropriateness under the environmental condi- in limiting resources and harvestable underwa- tions obtaining. Conversely, it is deduced that terlight. These templates are suggested to rep- thespecies compostion that is typical in a par- resent the filterability of species by pelagic habi- ticular water body, or in a particular type of tat conditions: where light and nutrients are not water body, is biassed by the conditions typi- constraining, many species are potentially able cally obtaining. Moreover, other species that are to grow,given that suitable inocula are present. frequently present in the same specific environ- Successful species will have evolved rapid-growth, ments, as a result of simultaneous recruitment, exploitative life-history (C)strategies that are share common traits and are thus allied to the preferentially (r-) selected under these conditions. same trait-selected functional groups. Moving down the gradients of resource and of Phytoplankton communities can continue to availability is analogised to ever constricting fil- develop so long as nutrients and harvestable light tration of (R-orS-) specialisms that will be are available to sustain it. Once either capacity increasingly K-selected by the ever more exacting is exceeded, however, recruitment rates weaken. constraint. Adaptive traits representing greater affinity for Analysing the mechanisms behind the observ- thelimiting factor, or greater flexibility in access- able patterns, the near ubiquity of common phy- ing or overcoming the deficiency assume pre- toplanton species is deduced to rely on efficient mier importance. Species with the appropriate and highly effective dispersal mechanisms. These traits to withstand the deficiency survive while are comparable to those of bacteria, some pro- populations of more generalist species stagnate tists and the micropropagules of sedentary inver- or regress. Competition for the limiting factor tebrates. The ability of phytoplankters to reach works against species richness. Given sufficient suitable habitat soon after it becomes available time, competitive exclusion leaves only the supe- means that their ecological behaviour is readily rior contender. describable in the terms of island biogeography This mechanism underpins the long- (MacArthur and Wilson, 1967). recognised process of succession. The equally The assembly of biomass by colonist species long-standing desire to explain successional (ascendency) is subject to the flux of energy and sequences of species composition are found to be carbon, and the size of the base of resources unhelpful. Autogenic maturation of communi- that is available to sustain a supportable biomass. ties is exposed to disruption by allogenic physical The standing mass and abundance of phyto- or chemical forcing. Community structure may plankton is also influenced by the fate of pri- resist or recover in the wake of such episodes, or mary product – to metabolism, or to the loss the community is restructured through a forced of intact cells by sedimentation or consumption replacement of biomass and dominant species by phagotrophic or parasitic heterotrophy. There by others more suited to the new conditions. remains a strong element of fortuity about phy- The response is disturbance. Such disturbances toplankton composition, what has arrived, how imposed at a frequency of two to four algal well it can function there (or how well it is generation times contribute to the endurance of allowed to do so). However, accumulating pop- high levels of diversity. ulations interact, with dynamic consequences. The diversity of phytoplankton, for so long Assembly becomes increasingly contingent upon considered paradoxical, is found to be main- thesum of accumulating behaviours, conform- tained by a combination of variable forces – envi- ing to patterns (‘rules’) summarised in Table 7.8. ronmental oscillations (habitat instability), more Of those present, the species initially likely to severe disturbances and recovery from catas- become dominant are those likely to sustain the trophic forcing – backed by the powerful disper- fastest net rates of biomass increase. These will sive mobility of organisms. Chapter 8

Phytoplankton ecology and aquatic ecosystems: mechanisms and management

aging, flight, reproduction) that contribute to the 8.1 Introduction survival and genomic preservation of the consumer species in question. In thermodynamic The purpose of this chapter is to assess the terms, the food web serves to dissipate as heat role of phytoplankton in the pelagic ecosystems that part of the solar energy flux that was pho- and other aquatic habitats. The earliest suppo- tosynthetically incorporated into chemical bonds sitions to the effect that phytoplankton is the (see p. 355). ‘grass’ of aquatic food chains and that the production of the ultimate beneficiaries (fish, birds and mammals) is linked to primary productiv- 8.2.1 Fate of primary product in the ity are reviewed in the context of carbon dynam- open pelagic ics and energy flow. The outcome has a bearing Based upon this simple premise, the performance upon the long-standing problem of phytoplank- of pelagic systems can be quantified in units of ton overabundance and related quality issues in energy dissipated (or of organic carbon reduced enriched systems, its alleged role in detracting and re-oxidised) per unit area per unit time, by from ecosystem health and the approaches to its abiomass also quantified in terms of its organic control. carbon content (or its energetic equivalent) and The chapter begins withanoverviewofthe partitioned according to function (primary pro- energetics and flow of primary product through ducer, herbivore, carnivore, decomposer). For the pelagic ecosystems, especially seeking a reap- open sea and the open water of large, deep lakes, praisal of the relationship between biomass and thescales of the input components and the rates production. at which they are (or can be) processed have been established in the preceding chapters. In Sec- tion 3.5.1,the attainable net productive yield of 8.2 Material transfers and energy pelagic photosynthesis, across a wide range of fer- tilities, was suggested to be typically in the range flow in pelagic systems 500–600 mg C m−2 d−1 (the thickness of the photic layer compensates for differences in con- One of the essential components of ecological sys- centration of photosynthetic organisms). Extrap- tems is the network of consumers that exploit olated annual aggregates (in the order of 100–200 theinvestment of primary producers in reduced gCm−2 a−1)agreewellwiththegeneralised find- organic carbon compounds. Some of these are re- ings of oceanographers for the open ocean, as invested in consumer biomass but much of the well as those deduced from satellite-based remote food intake is oxidised for the controlled release sensing (Section 3.5.2). On the other hand, they of the stored energy in support of activities (for- clearly underestimate the cumulative production 388 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

in many small to mediumlakes,aswellasin product may be exported to the sediments (but what were referred to as ‘oceanic hotspots’. Even generally ≤100 g C m−2 a−1)(Jonasson,´ 1978), so, from an investment of PAR of some 40 kJ to be processed there by benthic food webs. −1 (g Corg) ,thesynthesis of even this amount of By subtraction, the potential yield of primary photosynthate (4–8 MJ PAR m−2 a−1)isacknowl- product available to pelagic microzooplankton edged to be just a tiny fraction of the annual or to herbivorous mesozooplankton can scarcely harvestable PAR flux (less than 1% of the solar exceed 80% of the annual primary production energy flux) (Section 3.5.3). So far as its role in (say, 30–150 g C m−2 a−1)(Callieri et al., 2002). supplying the conventional energy requirements Even these consumer pools turn over much of the of the dependent food chain is concerned, biolog- carbon that they harvest in a matter of days; the ical turnover represents only a small proportion proportion that is available to larger metazoans of the dissipative flux. (10–25%; now rather less than 40 g C m−2 a−1,or At the same time, it is evident from the <1.6 MJ m−2 a−1) (Legendre and Michaud, 1999) modest year-to-year changes in the photosyn- is yet smaller. The balance is, of course, respired thetic biomass in the open sea that there is lit- to carbon dioxide. tle net accumulation of primary-producer mass or carbon. Taking chlorophyll levels of 20–40 mg chla m−2 to be typical for the trophogenic zone of 8.2.2 Food and recruitment of consumers the tropical ocean, phytoplankton standing crops in relation to primary production remain steadfastly constrained, probably in the It is nevertheless worth emphasising again that range 1–5gcellCm−2 (0.04–0.20 MJ m−2). Phy- theflow of energy and materials to higher toplankton concentrations in oligotrophic, high- trophic levels in the pelagic is a function of car- latitude lakes may be lower still (in some cases, bon turnover rate and not of biomass per se. ≤0.5gCm−2) (Section 3.5.1). These obdurately However, it is also relevant to remind ourselves low levels of producer biomass (B), like the pro- that the general uniformity of the pelagic out- duction (P)ityields, are deemed indicative of the puts (90 ± 60gCm−2 a−1)isofasimilarmag- ‘unproductive’ nature of the nutrient-poor sys- nitude to the rate of invasion of the water col- tems. Yet, as pointed out (Section 3.5.1), a P/B umn by atmospheric carbon dioxide (see Section yield of not less than 100 g C from not more 3.4.1). The fastest rates envisaged (up to 310 mg than 5 g cell carbon represents an extremely high Cm−2 d−1,or≤110gCm−2 a−1)depend upon biomass-specific productivity! winds that blow more strongly and more con- Low areal biomass and low cumulated pro- tinuously than is generally the case. They also duction are traditionally attributed to resource require a steep diffusion gradient from air to poverty. Without a simultaneously available fund water, caused by severe depletion of CO2 in solu- of other elements, including nitrogen, phospho- tion. With due allowance for turnover of the car- rus, iron and other traces especially, new biomass bon by the cycling between photosynthesis and and new cells cannot be built and recruited. respiration, it is feasible that the capacity of CO2- In the ocean and, to a large extent, in deep, limited pelagic primary production to sustain oligotrophic lakes, very little of the photosyn- new secondary production can be up to about thetically fixed carbon is deployed in new algal 40 g C m−2 a−1 but scarcely much more. biomass: as much as 97% may be vented from The exploitation of even this meagre supply of the active cells (Reynolds et al., 1985). Some of particulate organic carbon by mesoplanktic con- this is respired to carbon dioxide but a propor- sumers depends upon successful foraging. This, tion is released as DOC (see Sections 3.2.3, 3.5.4). in turn, depends upon adequate encounter rates This is processed by bacteria, whose own respira- of suitable foods by consumers, which is often a tion may account for 20–50% of the carbon thus function of food concentration. The range of con- assimilated (Legendre and Rivkin, 2000b; Bidanda centrations of suitable food organisms providing and Cotner, 2002). In smaller oligotrophic lakes, theencounter rates representing the minimum asignificant proportion of the original primary and the saturating levels for diaptomid copepods MATERIAL TRANSFERS AND ENERGY FLOW IN PELAGIC SYSTEMS 389 is suggested to be 5–80 mg C m−3 (Section 6.4.3) 2000b). The amount of food required to cover the (say, ≥5gCm−2 in a 100-m layer). This is sustain- maintenance of body mass is about one-third the ◦ able on a productive turnover of 100 g C m−2 satiating ration at 18 C, rising to about 50% at ◦ a−1,inthe sense that it could yield up to 40 temperatures below 10 C. gCm−2 a−1 and 1.6 MJ m−2 a−1 to consumers. From these data, we may compare the approx- Supposing this was invested entirely in the pro- imate ranges between the minimum and maxi- ◦ duction of diaptomids, a potential turnover of mum food requirements of trout at about 18 C − − some 10 × 106 1-mm animals m−2 a−1 (or 2 ×106 (2–7 kJ d 1 foran11-g fish, 25–75 kJ d 1 fora250- ◦ 2-mm animals m−2 a−1)maybeprojected from gfish), and at temperatures below 10 C (0.4–1.5 − − the data in Box 6.2 (p. 281). Depending upon kJ d 1 for an 11-gfish,5–15kJd 1 fora250-g fish). the depth of the mixed layer and the gen- Were these energy requirements to be derived eration times of the copepods, the sustain- exclusively from copepods, a slightly lower intake − able recruitment is in the order of 100–1000 is required (Diaptomus yields ∼23.9 kJ g 1 dry animals l−1 a−1. weight) (Cummins and Wuychek, 1971). However, − What kind of resource is this to planktivorous to consume a minimum of 0.08 g d 1 of cope- ◦ − fish? The foods, feeding habits and bioenergetic pod (for an11-gfish at 18 C), or upto3.1gd 1 requirements of several commercially important (for a 250-g fish), requires very efficient foraging. species are relatively well studied. The models Referring to the data in Box 8, between 2500 to of Kitchell et al.(1974, 1977)andPost(1990) 100000 2-mm calanoids would need to be cap- have been widely applied in fish management. tured and eaten each day or between 13000 and The work of Elliott (1975a, b)showedparticu- 500000 smaller (1-mm) animals. Given potential larly well how the maximum rate of growth of copepod recruitment rates equivalent to 10 ×106 − − − − brown trout (Salmo trutta)varieswithtempera- 1-mm animals m 2 a 1 (say 27.4 ×103 m 2 d 1), ture and with the quantity of food (Gammarus) theplanktivorous 250-g trout would have to har- consumed, within the range between total satia- vest the entire daily production under 18 m2 of tion and the minimum needed to balance basal surface (i.e. up to 1800 m3 of water) in order to metabolism. These have also been the subject of fulfil its maximum growth rate. Just to maintain sophisticated modelling (Elliott and Hurley, 1998, its body mass, it would have to forage the entire 1999)that simulates the earlier observations of copepod production from under 6 m2. performance of trout feeding upon invertebrates Though plainly approximations, they serve (Elliott and Hurley, 2000b)andreflects differ- to show two things about the scale of demand ences when other food sources are offered (Elliott of planktivory. First, that truly pelagic sys- and Hurley, 2000a). Information based upon only tems, exchanging carbon only with the atmo- one species of fish is not assumed to apply to all sphere, are bound to be oligotrophic and capa- others but the data serve to establish some impor- ble of sustaining only very low densities of tant deductions about pelagic foraging. The max- fish (averaging, perhaps, in the order of 1–10 − imum growth rate (and, hence, the maximum gfreshweight m 2). Second, that the ability satiating food intake) of all sizes of trout inves- of large pelagic consumers to harvest planktic tigated increased roughly fivefold between 5 ◦C production really does require specialist forag- and its maximumataround18◦C, before taper- ing adaptations. Indeed, pelagic feeding herring- ing off quickly at temperatures >20 ◦C. Growth- like fish (clupeoids), including shads, freshwa- saturating food intake was absolutely greatest in tersalmonids, coregonids (whitefish and ciscos) the largest fish examined (250 g), being equiva- and tropical stolothrissids, are all characteris- lent to ∼4.5 g Gammarus d−1,or∼75 kJ d−1 or tically strong swimmers, capable of covering ∼1.9gCd−1.Weight-for-weight, however, small vast distances in the near-surface layer. All have fish eat more, 11-g fish consuming up to 400 mg large gill rakers that confer enhanced capabilities Gammarus d−1,orabout7kJd−1.Ineithercase, forstraining small particles from several cubic the efficiency of conversion of ingested carbon metres of water passed over the gills each day. to trout biomass is 30–35% (Elliott and Hurley, To adult fish of almost all other species, pelagic 390 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

planktivory is normally a nutritionally unreward- Section 3.4.1 and cited work of Cole et al.(1994) ing means of foraging. and Richey et al.(2002). To be a net source of carbon dioxide (outgassing) also indicates that the lake is oxidis- 8.2.3 Carbon subsidies in lakes and the sea ing more organic carbon than was fixed in In coastal and shelf waters, in estuaries and situ. The short-retention lake must be a repos- embayments and in small to medium-sized lakes itory of organic carbon from the catchment, (according to the dimensional ranges proposed delivered in the inflow. Particulate organic mat- in Section 7.2.3:inlandwaters of less than 500 ter (POM, of various sizes), derived from ter- km2 in area), cumulative net primary production restrial ecosystems, especially including anthro- often exceeds the 100–200 g C m−2 a−1,some- pogenic interventions (agriculture, industries, times considerably so. Values as high as 800–900 settlements) is transported in abundance by gCm−2 a−1 have been reported (see Section 3.5.1). inflowing streams and rivers. Yielding slowly to Primary production at these levels is possible in microbial decomposition in the receiving water one or both of two ways. One arises through a (or, more likely, on is bottom sediments), this much-accelerated metabolic turnover of carbon material releases its component carbon dioxide synthesis and respiration; the other is the result in solution. Quantification of these contribu- of the system receiving additional carbon from tions is still in relative infancy. External POM, external sources. Such subsidies come in various derived mainly from the terrestrial plant pro- forms but theirprovenanceislargely from terres- duction of open moorland, was shown to be an trial sources. They are tangible in the sense that important food source in the oligotrophic, base- they supportfinitesedimentary fluxes, known poor water of Loch Ness, Scotland, UK. Analysing to amount to 100–300 g C m−2 a−1 in partic- seasonal variations in the stable-isotope composi- ular eutrophic lakes (Jonasson,´ 1978). Inflowing tion, Grey et al.(2001)determined that the crus- rivers are generally well equilibrated so far as tacean zooplankton, dominated by Eudiaptomus their dissolved carbon dioxide content is con- gracilis,derives some 40% of body carbon through −1 cerned (typically 0.5–1.0 mg CO2 L ,or∼0.15–0.3 ingestion of allochthonous particles; only the gCm−3)(seeSection 3.4.1). Delivered to the sea late-summer population of filter-feeding Daphnia or to the inland water in solution, it is also seems to derive most of its nutrition through immediately available for photosynthetic uptake. autochthonous pelagic producers. External POC Maberly’s (1996)investigation of the carbon spe- sources are likely to be relatively less important ciation in Esthwaite Water, a small (1.0 km2), in large lakes. Ozero Baykal is functionally olig- eutrophic, soft-water lake in the English Lake Dis- otrophic, where at least 90% of the annual car- trict (Section 3.4.1), showed that the lake received bon and oxygen exchanges take place in the open much more of its inorganic carbon in the inflow pelagic. However, external POC sources should streams than directly from the atmosphere. This not be discounted. Even in a lake as large as is despite phytoplankton-driven summer episodes Michigan, stream and groundwater inputs con- of high pH and CO2 depletion when the atmo- tribute as much as 20% of the usable carbon sup- sphere became the principal source. For most ply to the ecosystem (Bidanda and Cotner, 2002). of the year, pH is near neutral and the concen- Interestingly, the largest component of terrestrial tration of free CO2 in the lake is close to 0.12 organic carbon contributed to lakes and seas is mol m−3 (1.4gCm−3,oruptoseventimesthe often dissolved humic matter (DHM) (see Section atmosphere-equilibrated concentration). Far from 3.5.4)and, at first sight, the most likely subsidy relying on CO2 invasion from the atmosphere, to bacterial metabolism and the microbial food the net flux is in the opposite direction, the web. Although some DHM is amenable to bacte- lake venting CO2. This relative importance of the rial degradation, the metabolic yield, in terms inflows in supplying inorganic carbon is likely to of both energy and liberated carbon dioxide, is be general among lakes wherever the inflows dis- generallyslight (Tranvik, 1998), and production place the lake volume in less than a year (see also in oceanic bacteria remains more constrained by MATERIAL TRANSFERS AND ENERGY FLOW IN PELAGIC SYSTEMS 391 the turnover of carbon than nutrients (Kirchman, that shallowness also assists the concentration of 1990). areal production and of the founding resources, Frequent recycling of inorganic carbon should grants to shallow systems the opportunity to be relatively neutral in the carbon profit-and-loss recycle raw materials efficiently and nearly accounting. When the same atoms of carbon are continuously. first incorporated into carbohydrates and then Shallow lakes (and the shallow margins of released in algal, bacterial or microplanktic res- deeper ones) also offer potential habitat to macro- piration, the net yield is tiny in comparison to phytic vegetation, which, once established, alters the amount of carbon fixed. When this happens the turnover, internal stores and the direction several times in a year, the aggregate of fixa- and dynamics of carbon pathways. Rooted lit- tion (say 100gCm−2)may still have contributed toral plantsfixcarbonintocarbohydrates but, little in the way of either producer output or unlike phytoplankton, they generally have the export (perhaps <20 g C m−2). The balance (≤80 ability to retain and store carbohydrate poly- gCm−2)wouldhavebeenfixed, respired and mers within their tissue, rather than venting refixed several times over. In this case, the 20 g C it back to the water. Through their rooting sys- may have reached the bodies of large pelagic tems, they have potential access to nutrients nec- animals or have been consigned to the basal essary for protein synthesis that are not avail- sediments. able to phytoplankton. Relatively slower cycles Much of the carbon fixed in biomass at the of growth, maturation, death and decomposition bottom end of the trophic web is actually still also contribute to the long retention of resources quite labile, with about two-thirds of it being in biogenic products. Macrophytes may also pro- restored to inorganic components in less than a vide substratum for epiphytic algae as well as year (Jewell and McCarty, 1971)(seeSection 6.6). It habitat and nutritional refuge for a wide vari- is interesting that, in the open sea, much of that ety of benthic invertebrates – herbivores, detri- process takes place in the upper 200 m, before tivores and their predators. Littoral and sublit- the material has passed into the more permanent toralbenthos also offer far more attractive for- depths, whence its subsequent return may be aging opportunities to most fish, mainly because very delayed indeed. In many small to medium- potential prey organisms are both larger and dis- sized lakes, however, planktic cadavers may reach tributed more nearly in two dimensions rather the bottom of the lake within 200 m of the sur- than three. The reward of 4 g of Gammarus or face. Here, they are substantially protected from Asellus is considerably more attainable to a 250-g turbulent re-entrainment and they stay more or trout than gathering the same mass of zoo- less where they settle. Though persistently low plankton. Offshore sediments, supplied in part temperatures and a lack of oxidant in the inter- by autochthonous organic carbon from the phy- stitial water (and perhaps the bottom part of the toplankton, also nourish detritivore-based chains adjacent water column) may considerably slow of invertebrate consumers. These too mediate an the rate ofdecomposition, benthic detritivory, alternative producer–fish trophic link, passing by bacterial decomposers and bacterivorous proto- wayofbenthic macroinvertebrates, and avoid- zoa nevertheless continue to mineralise sedimen- ing the tenuous bridge of a diffusely dispersed tary organic material and release inorganic car- zooplankton. bon. The return of carbon and other inorganic Empirical comparisons of the biomass and elements to the trophogenic layers is extremely production of successive trophic levels in slow when compared to the open sea. However, lakes of various depths and trophic states in shallow lakes, where the bottom sediments have been used to determine the strength of are in direct contact with the trophogenic layer phytoplankton–zooplankton linkages. Many fac- and are liable to frequent entrainment by pene- tors are involved but energy-transfer efficiencies trating turbulent eddies (Padisak´ and Reynolds, are found to be generally greater in deep lakes 2003), recycling of sedimentary materials back to than in shallow lakes, where the alternative path- the water column is greatly facilitated. The fact ways are more likely to be available (Lacroix et al., 392 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

1999). Where higher consumers are involved, ments from2m3 and the 11-g animal could be modern techniques invoking the determination fully sated by clearing 200 L d−1. of the ratios of stable isotopes in the body mass Under these circumstances, feeding on zoo- and the foods of predators reveal much about plankton once again becomes a reasonably the principal pathways exploited. In a recent rewarding foraging option. The progressive overview, Vadeboncoeur et al.(2002)wereableto switching between benthivory and planktivory confirm the relative importance of zoobenthos in the feeding of young roach (Rutilus rutilus) in the diets of a wide variety of adult fish from in response to the abundance of planktic crus- lakes in the north temperate zone. In their bioen- taceans, as revealed by Townsend et al.(1986), has ergetic analysis of the fish production in the been highlighted earlier (see p. 278). The thresh- large tropical Lac Tanganyika, Sarvala et al.(2002) old of ∼1gm−3 zooplankton carbon is not a fixed showed that the non-clupeid species were sub- one but the behaviour helps to explain the coex- stantially supported other than by planktivory. istence of moderate concentrations of crustacean Copepods were the principal food only of the zooplankton and potential fish predators. dominant Stolothrissa tanganicae; alternative foods It is worth emphasising again that, quite also featured in the diet of another clupeid, Lim- apart from the habits and preferences of the nothrissa miodon. adults, the quasi-planktic 0+ hatchlings and juve- Although benthic pathways probably provide niles of a wide range of non-pelagic fish species the dominant link in the production of most feed almost exclusively in the plankton (Mills and species of fish in many small and medium- Forney, 1983;Cryeret al., 1986). Seasonal peaks sized waters, zooplankton may still be readily of phytoplankton production and zooplankton exploited where and when it is abundant. High recruitment, especially the vernal pulse in tem- concentrations of microzooplankton are neces- perate lakes and marine shelf waters, provide sarily sustained by correspondingly high avail- the major feeding opportunity to young-of-the- abilities of appropriate particulate organic car- year fish. Generally, they are recruited in large bon, which include fine detritus, bacteria, micro- numbers to the pelagic, often coinciding with zooplankters and, especially, planktic algae. Algal the maximum recruitment phases of zooplank- abundance requires not just the subsidised car- ton. Survivorship is generally poor but individual bon fluxes but the additional biomass supportive growth is potentially rapid. In temperate lakes, capacity provided by an ample nutrient supply. therates of recruitment and mortality experi- Concentrations of ingestible algae (nanoplank- enced by the young-of-the-year are closely cou- ters and small microplankters, generally <25 µm) pled to the seasonality of planktivore activity (see p. 267)substantially greater than 100 mg and the optimal exploitation of the zooplankton − Cm 3 are adequate to support growing popula- resource (Mills and Forney, 1983;Schefferet al., tions of filter-feeding daphniids. These can grow 2000). quickly and recruit further generational cohorts, At the same time, planktivory inevitably in a matter of days rather than months. With- depresses the numbers and impacts upon the out predation, daphniids can go on to achieve size distribution and recruitment rates of the aggregate filtration rates that may well exhaust zooplanktic prey. On the basis of quantities con- the food supply altogether. This level of filtra- sidered in this section, sustainable planktivory tion capacity may be developed by 20–30 large might yield between 10 and 100 g C m−2 a−1 − (∼2-mm) or 200 small (∼1-mm) Daphnia L 1 to consumers, depending upon the quality of (Kasprzak et al., 1999)(seealsop.267). Multiplied zooplankton nutrition. Planktivory also has an by the respective carbon contents (Box 6.2), the upper limit of sustainability (in the sense of not equivalent biomass of filter-feeders is about 1000 exhausting the food supply): this may be encoun- − − − µgCL 1 (1gCm 3 or ∼40 kJ m 3 of potential tered in carbon-rich ponds at fish densities equiv- energy to a consumer). Now weighed against the alent to30gm−2 fresh weight (Gliwicz and Preis, requirements of Elliott’s (1975a)trout, the 250- 1977). Among planktic systems generally, direct gfish could expect to harvest its daily require- planktivory is likely to sustain mean biomass in MATERIAL TRANSFERS AND ENERGY FLOW IN PELAGIC SYSTEMS 393 the order 1–10 g Cm−2. Larger consumer masses are indicative of subsidies to the carbon produced in the pelagic.

8.2.4 The relationship between energy flow and structure in the plankton What emerges is that phytoplankton provides almost the unique capacity to supply carbon to aquatic food webs in large, truly pelagic systems of oceans and large deep lakes. They are unable to support a large biomass (as a consequence of resource poverty) and they support no greater net areal biomass production than the rate of turnover of dissolved inorganic carbon will allow. Terrestrial subsidy to the carbon may relieve somewhat the constraints upon carbon Figure 8.1 Carbon- and energy-flow constraints on the deployment: tangible production and biomass structuring of emergent pelagic communities. Accepting that recruitment yields can be higher but are no the amount and distribution of native carbon sources vary longer reliant on phytoplankton production. The over several orders of magnitude, phytoplankton composition varies with carbon dynamics, while the concentration of food smaller and the shallower is the water body, the particles determines the type and productivity of the greater istheprobability that the ecosystem ener- zooplankton and, in turn, the resource and its relative getics will be powered by the adjacent hydrologi- attractiveness to fish. Shaded areas represent the transition cal catchment, the weaker is their dependence but is generally close to a carbon availability of ∼0.01 mmol upon phytoplankton production and the more L−1 in each instance. Redrawn with permission from integrated are littoral and benthic pathways into Reynolds (2001a). the food webs. The predominant species and their organisational structures in the pelagic are thus closely level ofCO2 solution are exclusively the conse- coupled to the carbon dynamics of the entire sys- quence of withdrawal by photosynthetic organ- tem: oligotrophic and eutrophic systems are dis- isms at a rate exceeding replenishment and indi- tinguished less by nutrients than by the carbon cate the imminence of limitation of photosyn- fluxes and the types of organisms most suited thetic rate by the carbon dioxide flux. This sit- to their mediation. A provisional guide to the uation may be a rare occurrence in resource- apparent thresholds separating these structural deficient, oligotrophic, ‘soft-water’ systems that provinces was proposed by Reynolds (2001a)and are chronically unable to support high levels of is reproduced in Fig. 8.1. The various trophic biomass. It would be yet more rare in ‘hard-water’ indicators are shown against a logarithmically- systems typified by a bicarbonate-enriched aug- scaled spectrum of carbon availability (scaled in mented total carbon capacity. However, in either mmol C L−1;1mmolL−1 is equivalent to 12 case, a more ample supply of nutrient resources gCm−3)toregistercritical biological bound- not only sustains higher levels of biomass but aries. Thus, the first row represents the avail- places greater demands on the capacity to sup- ability of total CO2: concentrations higher than ply carbon dioxide. Thus, enrichment ultimately the air-equilibrium level of CO2 gas in water selects against phytoplankters with a low affinity are due to the reserve of dissolved CO2 main- for carbon dioxide (like freshwater chrysophytes) tained by internal recycling and external ter- and in favour of species (such as the group H1, restrial subsidy, as well as to the store of dis- LM and M Cyanobacteria) (see Tables 7.1 and 7.2). solved bicarbonate ions present. Instances where That the carbon capacity underpins the CO2 concentration falls below the air-equilibrium nature and abundance of the POC availability to 394 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

planktic consumers also prejudices the selection ‘habitat template’ to accommodate the favoured of zooplankton. Low POC demands the sophisti- life-history traits and ecological strategies of ter- cated location and flexible capture adaptations restrial communities. Reynolds (2003a)reviewed of calanoids; mechanised filter feeding is shown aseries of attempts to develop an analogous in Fig. 8.1 as being realistically sustainable only template for freshwater communities in a way above 0.008 mmol L−1 (0.10 g C m−3). The thresh- that partitioned quantitatively the distinguish- old of zooplankton abundance for planktivory to ing thresholds (or controlling nodes). be attractive to adults of non-specialised species The outcome is presented as Fig. 8.2.Against of freshwater is inserted at about the same level. logarithmically scaled axes representing the Zooplankton populations at any lower concentra- resource constraints upon supportable biomass tions can only be of interest to specialised plank- and the processing constraints upon the rates ton feeders and send non-specialists inshore, to of its assembly, the space is divided up accord- forage for benthos. ing to the most likely limitations regulating There have been other important attempts thesystem. The resource axis is the easier to relate species structures or, at least, the to explain, with the upper limit of biomass dominant functional traits of ‘keystone’ species, depending upon the lowest relative bioavailabil- to given habitats. Setting zoogeographical con- ity of nutrient (corresponding stoichiometrically straints to one side, habitat characteristics pro- scaled axes for bioavailable N and P are inserted). vide the most relevant filter of regional (or γ-) Low resource availability is thus the key to habi- diversity (see Section 7.3.3). This has been demon- tats in which the elaboration of biomass usually stratedstrikingly in the species structure of local confronts ‘nutrient-limiting’ conditions. The pro- fish assemblages in different parts of contiguous cessing axis is constructed on the basis of photo- rivers and to be strongly predictable from their synthetic assimilation rates and their various adaptive traits (Lamouroux et al., 1999). At the dependences upon the fluxes of phota and inor- level of primary producers, the direction and fate ganic carbon. Towards its right-hand side, assem- of carbon is integral to the opportunities for its bly rates of primary producers and their depen- use and the adaptive traits that are advantageous. dent heterotrophs and phagotrophs are light- The conceptual explanations originally proposed dependent and critically constrained by mod- by Legendre and LeFevre (1989) and based upon est harvestable PAR fluxes (‘photon flux-limiting’ hydrodynamical singularities have been refined conditions). Moving leftwards, photosynthetic progressively to a model of regulation by food- assimilation rates become light-saturated but the web ‘control nodes’ (Legendre and Rivkin, 2002a). carbon-flux capacity is increasingly strained to In essence, the size and the trophic structure of the limits of the invasion rate of carbon diox- themarine plankton direct the flow of carbon ide from the atmosphere and the various catch- through particular, optimised channels (cycling ment sources of carbon. With increasing exter- in the web, export to the benthos or bathypelagic, nal sources of organic carbon, rates of processing etc.). The ‘deciding’ species structures are those moves from being less dependent on the carbon whose functional traits best fulfil the opportuni- supply and more so upon the supply of oxidant ties of the habitat. needed to make it available. The idea that the habitat is the best predic- These axes describe the space available to tor ofthemost-favoured species traits, survival ecosystem components according to their pri- strategies and, thus, community structures has, mary adaptations and so define a template for of course, been around for some years (Grime, community structures (Fig. 8.3). The axes read- 1977; Southwood, 1977;Keddy, 1992). Put in the ily accommodate the typical distributions of the simplest terms, different communities comprise trait-separated functional groups of freshwater species having certain suites of common charac- phytoplankton (Table 7.1)among waters of given ters and their prevalence is related to particular habitat characteristics (see for instance Fig. 7.8) features of the habitat in which the communities favouring particular morphological and physio- occur. Significantly, Southwood (1977)proposeda logical adaptations (Section 5.4.5). In this way, the ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 395

Processing fluxes d/

/ / / / and the speed of processing opportunities. Poten- Figure 8.2 Log/log representation of aquatic habitats in terms of resource-supportable biomass (which, it is assumed tial plaktivores may also be plotted, habitual can be regulated by the stoichiometrically least available pelagic-feeding fish are distinguished from typ- nutrient; nitrogen and phosphorus axes are included as ical benthivores in sediment-retaining habitats examples) and processing fluxes, which may be set by the (the psammophilic cyprinids) and those from less PAR income or the rate of carbon delivery or by the flux of silted habitats (lithophilic fish). The template is oxidative flux required to process the organic carbon also tentatively advanced to plot the distributions delivered. The area thus defined can be subdivided, as shown, of macrophytes (Fig. 8.3c) and benthos (Fig. 8.3d). according to the characteristic of the habitat thus defined (nutrient-limiting, carbon-limiting, etc.). Figure combines features of figures presented in Reynolds (2002b, 2003a). 8.3 Anthropogenic change in pelagic environments species characteristically dominating strongly nutrient-constrained systems (representatives of The habitat template of pelagic systems, invok- the Z, X3, A, E, F associations), those dominating resource and processing constraints, provides ing turbid or light-deficient environments (C, D, auseful bridge to understanding temporal vari- P and especially R and S species) and those cop- ation in stability and its consequences. We have ing with carbon-flux challenges in high-nutrient, already considered how seasonal changes in habi- high-light environments (X1, H, L)areseparated tat conditions alter the selection among stocks (Fig. 8.3a). The template similarly distinguishes of primarily C-, S-, or R-strategist phytoplankters (Fig. 8.3b) among planktic phagotrophs: the daph- (Section 5.5.4;seeFig.5.21), essentially as the niid, moinid and diaptomid traits signify dif- coordinates on the axes defining relative mixing ferent interplays in the availability of resources and nutrient are altered during the year. In the 396 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

Figure 8.3 Tentative use of the resource/processing tern of seasonal periodicity in the development habitat template to summarise the distributions of familiar and community assembly in the phytoplankton aquatic assemblages. (a) Phytoplankton shown by describes a series of loops tracking approximately trait-segregated functional groups (summarised in Table 7.2); similar courses through the habitat template. (b) representative functional groups of zooplankton and fish; The sketch in Fig. 8.4 shows a notional series (c) freshwater macrophytes; (d) freshwater benthos. CPOM, of such loops that, basically, follow the selec- coarse particulate organic matter; FPOM, fine particulate tion pathway ‘a’ in Fig. 5.21. There are modest organic matter. The figure follows ideas proposed in Reynolds interannual variations that may affect the num- (2003b). bers, relative abundance and occasional dominance changes of the phytoplankton in successive years. These loops could be said to be gov- model thus developed, variations in the nutrient erned by the various behavioural contols, act- availability were substantially the consequence of ing as Lorenzian ‘attractors’ (see, for example, biogenic activity but the physical conditions were Gleick, 1988). These defy randomness and are set, at least in part, by the external physical envi- variously susceptible to circumstantial weighting ronment. We have also extended this concept in of the dynamics of the individual species and, the context of predicted variations of unexpected thus, the communal outcome. Significant depar- magnitude or of variations at unexpected tempo- tures from this track, forced by extreme combi- ralintervals, sufficient to effect significant struc- nations of resource and processing opportunities tural disturbances (Section 7.3.3). Over a number (‘strange attractors’), then conform to convention- of years, interannual adherence to a basic pat- ally defined chaotic responses (Gleick, 1988, a. o.). ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 397

8.3.1 Eutrophication and enhanced phosphorus loading Defining the issues The problem of eutrophication (most especially of lakes) has been known for many years and, as a topic, has been discussed and reviewed in numerous previous publications. Here, the reader is simply referred to other works (Ryding and Rast (1989), is excellent) charting the history and the fascinating early attempts to explain the quite Figure 8.4 Sketch to show several annual sequences of the alarming increases in the plankton biomass that phytoplankton in a eutrophic lake, tracked as in Fig. 5.21,to were observed in a number of prime European show its Lorenzian attraction and the occasional chaotic, and North American lakes during the middle strange-attracted departure. part of the twentieth century. The background to the present section is that it mainly con- Many of the interannual differences in cerns the raising of supportive capacity of oth- seasonal dynamics of phytoplankton, from erwise clear-water lakes as a direct result of oligotrophic oceans (Karl et al., 2002)toeutrophic increased loadings of hitherto limiting nutri- lakes (Reynolds, 2002a), can be related to ents, arising from anthropogenic activities in the chaotic displacement of the environmental hydrological catchment. The problem is not con- attractors. It results in significant (though gen- fined to lakes as analogous enrichment of coastal erally rather temporary) variation in the driv- seas has enhanced their fertility several-fold sev- ing constraints, sufficient to evoke a series of eral with respect to the pre-agricultural period population responses. These summate to com- (Howarth et al., 1995). In both lakes and shelf munity responses, which, even if not precisely waters, eutrophication has led to alterations in explicable, may still be tracked in the habitat thespecies structure of the plankton and to what template. However, theremaywell be interan- are generally regarded as damaging changes to nual differences that are more insidious and aquatic ecosystems. more systematic, that occur in response to rel- Cultural eutrophication was defined by the atively slow progressive environmental in mor- Organisation for Economic Co-Operation and phometry, climate or in the anthropogenic influ- Development (1982)asthenutrient enrichment ences to which they are subject. Prior to mod- of waters resulting in the stimulation of an array ern concerns about accelerated climate change of symptomatic changes, among which are the as a consequence of human intervention in the increased production of algae and macrophytes, global carbon cycle (see Section 3.5.2), the first that are injurious to water quality, are undesir- two named sources were principally the concern able and interfere with other water uses. This of palaeoecologists, investigating the effects of definition distinguished the process from natu- postglacial sedimentary infill from catchments raleutrophication that many people associated subject to changing erosion rates and vegeta- with lake ageing, recognising that the undesir- tion cover. Environmental changes and system able changes were, in effect, merely some sort of responses over a few decades and within the acceleration. There are such things as naturally span of observation of individual laboratories eutrophic lakes (especially among kataglacial and, in some cases, of individual scientists may outwash lakes) (see p. 336)butmostof the be tracked from extant data collections. The palaeological evidence points to the opposite, most familiar of these changes havebeenthe that as natural catchments mature and support effects of eutrophication through anthropogeni- closed forest ecosystems, the nutrients released cally enhanced nutrient supplies and increasing decrease rather than increase. Sediment deposi- acidification of precipitation. tion diminishes the water depth and eventually 398 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

concentrates the nutrient load in a shallower are not optimised to give the best opportunity for depth of water, contributing positively to the theassimilation of nitrogen in proteins and plant apparent fertility of the water column. In this growth.Even so, loadings of nitrogen to lakes context, eutrophication (or its reverse, ‘olig- and coastal waters from agricultural catchments otrophication’) should be seen as no more than have probably been boosted two- to fivefold in the a contemporaneous reaction to contemporaneous last 50 years (cf. Lund, 1972). The use of phos- external nutrient loadings, which will exercise a phatic fertilisers has also increased over the same regulatory role so long as the nutrient is critical period, during which phosphorus levels in rivers, to the supportive capacity. lakes and seas have increased by a similar or It is also well known that the nutrient that still greater factor. However, the main phospho- is generally considered to act as the limiting ruspathway is probably quite different. Plants control is BAP (see Section 4.3.1). Actually, dis- ‘compete’ with soil chemistry for the phosphorus solved sources of assimilable nitrogen are just as applied, much becoming immobilised in the soil likely to be in short supply, relative to demand. by clay minerals, iron and aluminium hydrox- However, owing to the advantageous trait of ides and through co-precipitation with carbon- certain cyanobacteria to be able to fix atmo- ates (Cooke, 1976). Drainage from well-managed spheric nitrogen (Section 4.4.3), nitrogen-fixing pastures and cropfields generally tends to have a species may still be abletogrow,oftentolim- relatively low soluble-P content (there are plenty its imposed by the available phosphorus. This that are otherwise; see, for example, Haygarth leaves phosphorus still the principal regulatory (1997), although it may carry a substantial PP factor, even in nitrogen-deficient lakes (Schindler, load as eroded soil particles but which remains 1977). Deficiencies of micronutrients (Mo, Va, Fe) ‘scarcely bioavailable’ (cf. Table 4.1). On the other may prevent much nitrogen fixation (Rueter and hand, much phosphorus remains in the soil or Petersen, 1987) (Section 4.4.3). Availability of iron is incorporated into the biomass that is actually constrains the plankton-supportive capacity of cropped by consumers. large parts of the ocean (Section 4.5.2)but, with As a metabolite of consuming animals (includ- the exception of those instances where plankton ing humans), excess phosphorus is eliminated is simultaneously nitrogen-deficient and fixation- in solution (i.e. excreted as MRP). In the nat- constrained, phytoplankton in lakes is more ural way of things, this is most likely to be likely to be limited by phosphorus than any other returned to soils and to further chemical immo- nutrient. bilisation. Changing cultural standards, driven by Anthropogenic enhancement of phosphorus burgeoning human numbers, urbanisation and comes from several sources. The clearing of for- public health concerns, insist that most of that est, the promotion of agriculture and the use of ‘waste product’ is intercepted and subjected to inorganic fertiliser have been trade marks of a secondary biological treatment (in which much green revolution of food production on an indus- of the organic content is re-oxidised and re- trial scale. The ascendency of a human popula- mineralised). On average, adult humans excrete tion of over 6 000 000 000 would have been quite some 1.6 g P d−1 (0.58 kg P a−1) (Morse et al., 1993); unsustainable without this. Agriculture rejuve- with modern standards of secondary sewage nates ecosystem- and biomass-specific productiv- treatment, between 70% and 100% (Kallqvist¨ and ity but also opens them to resource exchange Berge, 1990)ofthis is returned to the aquatic (Ripl and Wolter, 2003). Often, deficiencies of environment in a readily bioavailable form. nitrogen have to be overcome in order to realise Historically augmented by soluble phosphates productive potential and, world-wide, applica- emanating from the hydrolysis of detergents tions of inorganic nitrogenous fertilisers repre- based on sodium tripolyphosphate (STPP; see sent a major component of agricultural practice. Clesceri and Lee, 1965)andboostedbyother Their high water solubility makes then vulnera- household wastes, domestic sewage has undoubt- ble to leaching in drainage water, if applications edly enhanced P-loads to rivers and pelagic ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 399 systems in general. Reynolds and Davies (2001) related mean summer chlorophyll a concentra- estimated human contributions to have con- tions to winter–spring concentrations of TP (Dil- tributed up to 1.6 kg P individual−1 a−1 in the lon and Rigler, 1974;Oglesby and Schaffner, recent past. Certain manufacturing industries 1975)ormaximum concentrations to vernal BAP also generate significant quantities of dissolved (Lund, 1978;Reynolds, 1978c)or, eventually, the phosphorus. However, in both its coincidence mean annual chlorophyll concentration to the with the implementation of widespread treat- annual P-loading factor (Vollenweider, 1975, 1976; ment and the statistical allocation of contribu- Rast and Lee, 1978). tions to the P budgets of contrasted river basins All these formulations yielded similar slopes (e.g. Caraco, 1995;Brunner and Lampert, 1997), (Reynolds, 1984a): the greater the phosphorus effluents from secondary sewage treatment are availability the greater is the phytoplankton most strongly implicated as the leading proximal biomass likely to be supported. However, it is the source of the phosphorus complicit in eutroph- Vollenweider–OECD approach which has been ication (Reynolds and Davies, 2001). Lest this most frequently applied as it incorporates the fur- is taken as an accusation, it must be recalled ther useful empirical step of relating in-lake avail- that modern agriculture and the socio-economic ability to the nutrient loading from the catch- structures that it sustains are founded upon the ment. The full formulation models the relation- enhanced distribution, chemical mobility and ship between average chlorophyll biomass and biotic dissipation of (e.g. Moroccan) phosphate theamount of phosphorus supplied to the lake, and (e.g. Chilean) nitrate. Whether these ele- adjusted to availability through corrections for ments are removed to water directly or through water depth and hydraulic retention. In its final a complex anthropogenic food chain is really form (Vollenweider and Kerekes, 1980), the regres- academic. What matters is that these pathways sion of the annual mean concentration of chloro- −3 are understood, that their impacts are quanti- phyll a ([chla]a,inmgm )isadirect function fied, and that they inform rational strategies for of an averaged, ‘steady-state’ index of phosphorus −3 improving their future management. availability (P,alsoinmgm ):

log [chla]a = 0.91 log[P] − 0.435 (8.1) Aquatic impacts of phosphorus loads to lakes The Organisation for Economic Co-Operation and The derivation of P is interesting and is Development (OECD) sponsored a series of co- extremely valuable when the management of P ordinated studies of the relationship between loads becomes an issue. It begins with the dynam- phytoplankton biomass (analogised to chloro- ical relationship between the total phosphorus −3 phyll a concentration) and phosphorus availabil- concentration in the lake water ([P], in mg m ) ity in lakes (TP was preferred to MRP, which, if and the rate of supply, less the amounts lost in limitation means anything, is rather scarce). The the outflow and to the sediments: first report (Vollenweider, 1968)uncovered the d[P]/dt = (q [P] )/V − w [P] − σ [P] (8.2) essence of a mathematical relationship between i i P P in-lake concentrations of chlorophyll a and TP where qi is the inflow rate and [P]i is the phospho- (although, in fairness, Sakamoto (1966)and rus concentration of the ith inflow stream and V Sawyer (1966) had each previously recognised is the volume of the lake; σ P is the phosphorus this). The final report (Vollenweider and Kerekes, sedimentation rate and wP is the rate oflossof 1980)provided definitive statistical fits of mean phosphorus in the outflow. At steady state, annual chlorophyll a concentration against the delivery of TP from the catchment (the ‘load- [P] ={L (P)/z}/{wP + σP} (8.3) ing’), corrected for the effects of depth and hydraulic replacement. In between, a flurry of where L(P) is the aggregate areal rate of phospho- other equations was published that (variously) rusloading (in mg m−2 of lake area per year) 400 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

and z represents mean depth. The most difﬁ- cult term to estimate without detailed measurement is the phosphorus sedimentation rate; Vol- lenweider (1976)proposedanempirical solution in which: √ σP ≈ (z/qs)/tq (8.4)

where tq is the hydraulic residence time in years, calculated as lake volume (V)divided by the annual sum of the inﬂow rates ( qi), and where qs is the hydraulic loading rate (in m −1 a ), approximately equivalent to z/ tq.Rewriting Eq. (8.4), √ √ σP ≈ [z/(z/tq)]/tq = (1/tq)/tq (8.5)

Supposing that wP = 1/tq,Eq.(8.4)maynowbe Figure 8.5 The Vollenweider–OECD relationship between rewritten average chlorophyll a concentrations in lakes and the √ phosphorus availability inferred from loading characteristics, [P] ={L (P)/z}/{1/tq + (1/tq)/tq} (8.6) with 99% confidence limits. The equation (8.8,inthe text) of the fitted line relates chlorophyll to mean in-lake phosphorus Multiplying out by t gives q concentration (log [chla]a = 0.91 log P – 0.435, where P √ is derived as P ={L(P) / qs} / {1 +(z / qs)} (see text and tq[P] ={L (P)/z}/{1 + [z/(z/tq)]} Eq. 8.7). Redrawn with permission from Reynolds (1992a). and cancelling √ [P] ={L (P)/qs}/{1 + (tq)} is, the log–log format obscures a wide variation or √ in real average chlorophyll content for a given [P] ={L (P)/qs}/{1 + (z/qs)} (8.7) derivation of [ P]. For instance, a literal extrapolation of Fig. 8.5 is that the average chlorophyll The log–log relationship of chlorophyll con- supported in a lakehavinganavailabilityindex centration to Vollenweider’s index of phospho- of 100 mgPm−3 may be predicted, with 95% rus availability ( P)isplotted in Fig. 8.5. confidence, to be between 10 and 53 mg chla The fitted regression is thus the definitive m−3.Onthe other hand, the Vollenweider–OECD ‘Vollenweider–OECD model’; restated, model is a powerful, empirical statement of the

log[chla]a = 0.91 log[{L (P)/qs}/ long-range performance of large and medium- √ sized lakes subject to varied differing phosphorus {1 + (z/q )}] − 0.435 (8.8) s loadings. Great store has been placed on this formulation. Reducing the relationship back yet more Some authors have apparently been perplexed towardsasemi-quantitative word model, the by sites which do not concur with the regression Organisation for Economic Co-Operation and (such outliers are evident in Fig. 8.5)andhave Development (1982)proposed approximate phos- sought amendments to the equation in respect of phorus availabilities to coincide with the trophic- other influences, including the effects of grazers state, metabolic-dependent categories of lakes (e.g. Prairie et al., 1989). Were serious criticisms in use since the days of Naumann (1919). The to be made, they might be directed at the origi- slightly modified scheme of Reynolds (2003c), nal and inadvertent bias towards deep temperate incorporating the continuing prevalence of phos- lakes. Had more shallow, heavily loaded, P-cycling phorus limitation is shown in Table 8.1. or well-flushed systems been considered, a less Such deductions help to inform practical satisfying result would have been obtained. As it approaches and strategies for the manipulation ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 401

Ta b l e 8.1 Proposed criteria for classifying lakes on the basis of trophic state and metabolic constraints, based upon OECD (1982) and Reynolds et al.(1998)

a [TP] or [P] Months where MRP Average [chla] Category (mg P m−3) <3mgPm−3 (mg m−3) Ultraoligotrophic <3Always <2 Oligotrophic 3–10 9–12 per year 0.7–4.5 Mesotrophic 10–35 4–9 per year 2–24 Eutrophic 35–100 <4 months per year 3–53 Hypertrophic >100 Never >10

a For predicting maximum chlorophyll yield from the bioavailable phosphorus, see Section 4.3.4 and Eqs. (4.14) and (4.15). of phosphorus loads. These are reviewed later chemicals, they had already achieved notori- (see Section 8.3.3). Mention may also be made ety for their tendency to form surface scums. of lake-specific derivations of the metabolic con- Accumulated by downwind drift, these paint-like sequences of varied external phosphorus loads. shore-line swathes of stranded algae are con- Supposing that the portion of the bioavailable sidered to be, at best, unsightly. As they die phosphorus load that is actually retained gen- and decompose, they release pigment into the erates a stoichiometrically equivalent mass of water and become evil-smelling. Thus, ‘leprous organic carbon and that this is oxidised by a sto- and fetid’ (Sinker, 1962), they discourage con- ichiometrically equivalent quantity of hypolim- tact with, enjoyment of and fishing from, the netic oxygen, Reynolds and Irish (2000)success- waters so affected. In point of fact, rather few fully simulated the differing impacts of the pro- species of Cyanobacteria do this: those belonging gressive eutrophication and its subsequent rever- to the‘bloom-forming’, gas-vacuolate genera that sal on the hypolimnetic oxygen content of the either occur in coenobial or colonial structures Northand South Basins of Windemere. (such as Microcystis, Woronichinia and Gloeotrichia; trait-separated functional groups L, M)orinfila- 8.3.2 Blue-green algae and red tides ments that aggregate in clumps or flakes (as in many Anabaena, Anabaenopsis and Aphanizomenon In both lakes and shelf waters, progressive species belonging to the H groups). Other gas- eutrophication has resulted not just in the vacuolate, filamentous forms that remain soli- maintenance of a higher average phytoplankton tary (Planktothrix, Limnothrix, some Anabaena and biomass but also to shifts in species composition Cylindrospermopsis of the S associations) can be that apparently favour Cyanobacteria (in lakes) abundant but rarely scum. Generally, small-celled and small dinoflagellates (in certain seas). Nei- species, including picoplanktic Cyanobacteria, do ther change is straightforward. In either case, not have gas vacuoles and, thus, have no means the change brings consequential effects upon of constituting surface scums at all. environmental quality and both, by coincidence, While such blooms are certainly not new carry implications for human health. Beyond (see Griffiths (1939)for a review), even entering that the direct causes of the problems are quite local folklore at locations where they have been distinct and are referred to separately. long recognised (Reynolds and Walsby, 1975), reports of scums (or blue-green algal blooms) Cyanobacterial ‘blooms’ became much more numerous since the mid Long before it was confirmed that certain species twentieth Century and appeared, often spectac- of Cyanobacteria (or blue-green algae) were ularly, in lakes where they had previously been capable of producing several extremely toxic virtually unknown. At first, their appearance 402 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

was attributed to sudden, unexplained bursts of temperate Cyanobacteria would be confronted rapid growth and replication (Mackenthun et al., by post-vernal phosphorus exhaustion. The his- 1968). In fact, the algae grow only relatively tory of eutrophication in Windermere (as told by slowly. They accumulate at the surface only dur- Reynolds and Irish, 2000)illustrates very well the ing quiet weather (minimal vertical mixing) and interannual stability of the silicon-constrained only as a consequence of their failure to regu- diatom crops despite year-on-year increases on late the buoyancy imparted by the gas vacuoles. annual P loadings. The record reveals the onset of From being well dispersed through the water col- late-spring P surpluses and the advent of signifi- umn, buoyant algae are disentrained to the sur- cant summer cyanobacterial blooms. It shows the face when the wind drops. Becoming thus ‘tele- demise of both in the wake of reduced phospho- scoped’ (Reynolds, 1971)fromdepthtothesur- rusloadings after 1992. Sas’ (1989)review of suc- face and further concentrated along lee shores cessful lake restoration schemes in Europe iden- by light winds, the scums give a greatly exag- tified a reduction in cyanobacterial crops in each gerated impression of abundance. Nevertheless, of several lakes, only after BAP levels had been the increasing incidence of blooms prejudicial reduced during the spring period to levels too to water quality correlates well with increas- low to support significant blue-green recruitment ingly enriched conditions, suggesting a power- during the early summer. ful causal link between increased abundance of bloom-forming Cyanobacteria with increased Cyanobacterial toxicity phosphorus availability (Gorham et al., 1974). Problems with cyanobacterial scums have been Indeed, such blue-green algal blooms have per- compounded by the recent ‘discovery’ (really it haps done most to give eutrophication its bad wasaconfirmation of a long-held suspicion) of name. their severe toxicity to humans. Again, the issue Interestingly, bloom-forming Cyanobacteria does not arise as a direct consequence of eutroph- need no more phosphorus to support growth ication but, on the other hand, the occurrence or to saturate their growth-rate requirements of toxic organisms in health-threatening concen- than other common eukaryotic algae (Reynolds, trations is dependent upon an enriched resource 1984a)(seealsoSection4.3.2 and Table 4.1). Nei- base. Cyanobacteria are not the only group ther does phosphorus availability guarantee blue- of phytoplankters to produce toxic metabolites: green algal abundance: they are relatively intoler- besides the ‘red-tide’ dinoflagellates (see p. 407 ant of acidity and low insolation (Table 7.2). They below), several kinds of marine and brackish hap- are extremely tolerant of high pH and may domi- tophytes (including Prymnesium and Chrysochro- nate where algal production generally strains the mulina)produce substances toxic to fish and other carbon supply (Shapiro, 1990). They commonly vertebrates. However, it is the self-harvesting in do well in mildly P-enriched calcareous lakes scums that so magnifies the potential harm that (Reynolds and Petersen, 2000). cyanobacterial toxins might pose to humans. Also relevant is the fact that the growth of the Many instances of sickness and death of live- ‘large’ algal units that characterise the bloom- stock and, occasionally, humans after consum- forming blue-green algae is especially sensitive ing water containing Cyanobacteria had been to lower temperatures (see Section 5.3.2 and Fig. reported over a number of years, especially from 5.3). At least so far as the well-studied temper- warm,low-latitude regions. It had been supposed ate lakes of North America and Europe are con- by many hydrobiologists working remotely that cerned, it became apparent that the offending these were symptomatic of putrescence and bac- bloom-forming species are excluded in the early terial pathogens. The possibility that the algae year by low temperatures. These are, of course, themselves could be harmful appears not to have no bar to the successful early growth of diatoms been taken very seriously, prior to the pioneer- and nanoplankters. By the time that the physical ing investigation by a small but active group of conditions are adequate for their growth, many scientists led by P. R. Gorham (see e.g. Gorham ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 403 et al., 1964). The work was continued by W. W. become dominant and its rivals have already Carmichael and his colleagues (see Carmichael been competitively excluded. It is possible that et al., 1985). Many of the present perspectives are thetoxicity is fortuitous and the compounds due to the efforts of G. A. Codd and his colleagues are the by-product of some unknown homeo- at Dundee (for a recent overview, see Codd, static step in the ageing of the cyanobacterial 1995). The eventual interest of the World Health cells. Toxicity of Microcystis was long suspected Organisation promoted the useful handbook by to be a symptom of stress in natural popula- Bartram and Chorus (1999). tions and which was reversible by introducing It is now well appreciated that Cyanobacteria colonies to nutrient-replete media under nor- are capable of producing at least three classes mal illumination and temperature (Carmichael, of toxins. The acutely hepatotoxic microcystins 1986). More recently, Orr and Jones (1998)pro- attack the digestive tract of consumers, causing vided convincing evidence that the production acute pneumonia-like symptoms and sickness in of microcystin in nitrogen-limited Microcystis cul- humans. More than 60 structural variants have tures is proportional to the cell-replication rates. been detected in cells or cell-free extracts from a Field evidence is inconsistent, at best suggest- range of cyanobacterial species, not just of Micro- ing that toxin production is sporadic. Jahnichen¨ cystis (K. Sivonen and G. Jones, in Bartram and et al.(2001), experimenting with Microcystis har- Chorus, 1999). It is believed that they act by block- vested from Bautzen Reservoir, Germany, showed ing phosphorylation; weight for weight, the toxic- that microcystin was synthesised only during the ity of microcystins is comparable to that of curare phase of exponential increase and only after the and cobra venom. The neurotoxic anatoxins are external pH exceeded 8.4, free CO2 was virtually also acute poisons. Chemically, they resemble exhausted and photosynthesis was drawing on thedinoflagellate saxitoxins, and are produced bicarbonate. The suggestion that microcystin pro- principally by the nostocalean genera. The third duction has some connection with the extreme group of toxic compounds are lipopolysaccha- affinity of cyanobacteria for carbon uptake (see rides: these are the least well characterised but Section 3.4.2)isanattractive proposition. It possibly the most insidious of the three, being is also far from incompatible with the earlier associated with sub-lethal skin irritations as a findings. consequence of contact with affected water or Toxicity per unit of Cyanobacterial mass with cumulative chronic effects of frequent expo- varies with the species of Cyanobacteria present, sure. thepotential of the resources to support their The benefit to the organisms of producing growth and the availability of DIC. However, the such poisonous chemicals is still an unexplained extent to which physical processes may have fur- paradox. It is scarcely a necessary defence against ther concentrated the cyanobacterial mass mag- herbivorous crustacean or ciliate consumers and, nifies the risk of human exposure to a toxic dose. besides, to kill potential grazers is as protective As has been stated, the microcystins are them- to other species of the phytoplankton as to the selves extremely toxic: the lethal intraperitoneal Cyanobacterium and most of these, it will be lethal dose to mice of the common microcystin- recalled, grow rather faster. There would be more LR is 1.25 µg/25 g (Rinehart et al., 1994), or 50 point to producing toxins against the other algae. µgkg−1.Itisnot assumed that all mammals There is some evidence for the suppression of are equally sensitive but, supposing it were simi- growth of common algae, either in media from lar, the generally lethal oral dose would be some which the cyanobacteria have been removed or 10- to 100-fold greater, i.e. in the order 0.5 to 5 in fresh medium, spiked with extract from spent mg kg−1.Swallowing 30–300 mg of microcystin Microcystis cultures (Reynolds et al., 1981). would probably be sufficient to kill a 60-kg adult. What is interesting about this is that the However, the mass of microcystin produced by toxin production seems most prolific at the time individual cyanobacterial cells is measurable in of population climax, after the organism has femtogram quantities. Lyck and Christoffersen 404 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

(2003)haverecentlymeasured∼85 ± 44 fg micro- reportedly harvested for food by natives of Chad: cystin per Microcystis cell in field populations, Pirie, 1969). I am not aware of a scientific study somewhat less than the 278 ± 115 fgcell−1 that that confirms my impression that most animals Christoffersen (1996) had measured in laboratory avoid drinking water tainted by Cyanobacteria cultures. Against the dry mass of the cell (aver- but there is certainly evidence that domestic live- age 32 pg; Table 1.3), microcystin accounts for stock may be reluctant to drink until overcome perhaps 1–1.5% of the typical dry mass (note, a by thirst (Reynolds, 1980b). It is noticeable that similar amount to its chlorophyll complement). fish and Daphnia also avoid water sullied by scum. Supposing the highest measured toxin content, All this makes the behaviour of domestic dogs – then the smallest number of Microcystis cells that which seem uniquely attracted to wallow and roll would havetobeingestedinordertodeliver in shoreline scums – quite difficult to explain. atoxic dose is close to 100 thousand million The attraction proves fatal when the animals (1011 cells) and, in all probability, ten times that start to lick their coats. amount. When compared to the dispersed cell Pets apart, there is a need to be concerned populations attained by natural Microcystis popu- about sub-lethal or chronic exposure to the lations noted in nature (my record is ∼360 000 toxic Cyanobacteria, not least through drinking cells mL−1 foranear-monospecific population in waterpurified from reservoir storages in which one of the Blelham enclosures and equivalent to planktic Cyanobacteria may be abundant. Treat- ∼120 mg chla m−3), it is clear that a toxic dose ment processes that remove planktic cells by is equivalent to scarcely less than 28 L of lake filtration, flocculation or dissolved-air scaveng- water. ing are effective in removing intracellular toxin One would be entitled to conclude that the but engineers need to be aware of treatments risk of drowning in the water far exceeds that that induce cell lysis and secretion of toxin into of poisoning by its suspended contents, but thewater. Cyanobacterial toxins are effectively for the phenomenon of surface-scum forma- removed from the water passed through gran- tion. Through the abrupt flotation of buoyant ular activated carbon. Reservoir managers are colonies to the water surface, the concentration also often able to select from several draw-off of Microcystis colonies hitherto dispersed through options, in order to avoid the intake of Cyanobac- adepthof∼5misquickly compacted (‘tele- teria. Current guidelines from the World Health scoped’: Reynolds, 1971)intoalayerno thicker Organisation suggest 1 µgmicrocystin L−1 as the than 5 mm (i.e. a 1000-fold concentration). The upper safe limit (see Bartram and Chorus, 1999). scum is further concentrated by subsequent drift If reservoir populations approached the toxicity toaleeshore, where the population from (say) a level observed by Christoffersen (1996), it has to 1-km fetch could be reasonably aggregated into be admitted that many reservoirs supply water ashoreline scum of 1 m or so in width. Now, supporting Cyanobacteria rather more numerous the microcystins are perhaps concentrated by a than the equivalent of 1 µgchla L−1. factor in the order of 106, capable of supply- Forrecreational waters, the hazard posed to ing the toxic dose within some 28 µLoflake swimmers, sailors and anglers alike remains the water! ingestion of scum. In addition to providing peri- The salutory deduction is that the shore- odic warnings, site managers usually seek a com- line scums are rather more threatening than promise between banning public access to water the dispersed populations. It is interesting that that they know may contain extant blue-green our species has coexisted with bloom-forming algae and allowing activities to continue until Cyanobacteria for some millions of years, mostly there is a significant risk of toxic algae aggre- oblivious to the latent hazard. On the other hand, gating along the shore. This equation is not just the scums are so uninviting that they invoke about how much alga is dispersed in the water the life-saving instinct of disgust: people are gen- but whether, and by how much, it is likely to erally dissuaded from consuming or contacting self-concentrate in areas of public access. Using this water by revulsion (although Spirulina is areverse calculation of what was needed to ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 405 generate a toxic dose in 28 L of lake water, quently dominate shallow, turbid lakes (Schef- Reynolds (1998c)started with what seemed like fer et al., 1997)andthat nitrogen-fixing Nos- areasonable estimate of a volume swallowed, tocales may dominate eutrophic lakes in defi- how many toxic cells that that might contain and ance of low levels of combined nitrogen, pro- how much that factor of concentration could be vided certain other conditions are satisfied (Sec- sustained by flotation and leeward drifting. The tion 4.4.3). Cyanobacterial abundance is, like that outcome for buoyant Microcystis suggested that a of most other forms, correlated to TP and TN lake population equivalent to 5 µgchla L−1 is a (e.g. Downing et al., 2001), not least because their level warning of significant risk and is a trigger biomass will account for much of the TP and for careful monitoring for downwind scums in TN that is present. In temperate lakes, growth calm weather. Most Anabaena, Aphanizomenon and of bloom-forming Cyanobacteria is slow in win- Woronichinia species. float up only half as rapidly, ter and they mayfailtogrowatallifthe permitting a doubling of the concentration trig- competitors (especially vernal diatoms) clear the gering the warning level. Planktothrix and Limno- waterofdissolved phosphorus before the light thrix float so relatively slowly that concentra- and temperature thresholds are past. Species that tions equivalent to 100 µgchla L−1 may betoler- overwinter on the benthos experience critical ated before warning levels are triggered. The dis- difficulties of seasonal recruitment (Reynolds persed cell concentrations of named Cyanobac- et al., 1981;Reynoldsand Bellinger, 1992;Bragin- teria equivalent to these warning thresholds are skiy and Sirenko, 2000;Brunberg and Blomqvist, set out in Table 8.2. 2003). If filter-feeders are abundant before the new colonies are released into the water col- Control of cyanobacteria umn, then grazing can be highly effective in Interest persists in being able to eliminate and/or stemming recruitment to the plankton (Ferguson exclude Cyanobacteria from managed water bod- et al., 1982;Reynolds, 1998c). ies or, at least, to keep their numbers at back- By deduction, effective controls against ground levels. Unfortunately, there is no simple cyanobacterial dominance are few. Low concen- or universal means to attack Cyanobacteria per trations of available phosphorus are beneficial se which is not likely to be destructive of all in temperate lakes (in the sense of not support- other biota, desirable or otherwise. Deep-rooted ing bloom-forming Cyanobacteria) but not so in suppositions about the nutrient requirements tropical lakes, especially if they stratify and have of ‘the Cyanobacteria’ and about their suscep- long retention times (see Section 7.2.3). Of gen- tibility to grazing rather ignore the very wide eral importance, however, is the poor tolerance diversification evident among the group of mor- by bloom-forming genera, especially Anabaena, phology, physiology and life history. Even when Aphanizomenon and Microcystis,ofentrainment in authors have focused on just the bloom-forming mixed layers that take the algae well beyond genera, they havetended to seek mechanistic the conventional photic depth and thus dilute explanations emphasising the importance of cer- and fragment their exposure to the light field. tain correlative factors, such as nutrient ratios This sensitivity was detected in the early liter- and biological interactions, in governing popu- ature reviews (Reynolds and Walsby, 1975), was lation dynamics (see e.g. Levich, 1996; Bulgakov verified in the mixing experiments of Reynolds and Levich, 1999;Elser, 1999;Smithand Ben- et al.(1983b, 1984) and was a demonstrable con- nett, 1999). Other analyses suggest that cyanobac- sequence of the application of destratification terial dominance is a more fortuitous outcome techniques in London’s Thames Valley Reservoirs of interacting factors that include perennation, (Ridley, 1970;Steel,1975). Since then artificial weather effects, column mixing and carbon affin- mixing techniques have been used widely in the ity (Reynolds, 1987a, 1989a, 1999b; Dokulil and protection of water quality in reservoirs (Steel Teubner, 2000;Downing et al., 2001). The main and Duncan, 1999;Kirke,2000); the reduction generalisations that are possible seem to be in cyanobacterial mass has been generally wel- that the filamentous group-S Oscillatoriales fre- comed, even where this was not the primary 406 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

Ta b l e 8.2 Approximate biomass equivalents of potentially toxic Cyanobacteria attaining a (‘warning’) level that could deliver a lethal oral dose to a human adult; the derivations assume that intracellular toxin content to be the highest reported at time of writing, that the organisms are at their most buoyant and that their horizontal aggregation is subject to surface winds of 3.5 m s−1.Developed from Reynolds (1998c).

Cells (or Suggested mm) warning Number of cells ‘Average’ mL−1 level (or mm) mL−1 Cell volume ‘Average’ cell chla to 1 µg(µg chla equivalent to Speciesa (µm3)b cell C (pg) (pg) chla L−1 L−1 warning level Microcystis 30 (65) 100 15 0.3 2 000–4 000 5 10 000–20 000 aeruginosa Woronichinia 5(40)75 10 0.2 4 000–6 000 10 40 000–60 000 naegeliana Aphanizomenon 5(12)20 3 0.06 15 000– 10 150 000–180 000 ﬂos-aquae 18 000 Anabaena 70 (100) 130 22 0.45 1 500– 10 15 000–30 000 circinalis/ 3 000 ﬂos-aquae/ spiroides Anabaena 33(47)113 11 0.22 3 000–6 000 10 30 000–60 000 lemmermannii Anabaena 270(400)520 90 1.8 400–700 50 20 000–40 000 solitaria Planktothrix 28 000 10 500 210 4–5.5 100 400–550 mougeotii∗ (46 600) (1 mm) 71 000 Planktothrix 12 000 (24 5 500 110 8–11 100 800–1 100 agardhii∗ 000) 28000 (1 mm) Limnothrix 1800 (3140) 700 14 60–80 100 6 000–8 000 redekei∗ 7500 (1 mm) Pseudanabaena 780 (1220) 275 5.5 160–200 100 16 000–20 000 limnetica∗ 1800 (1 mm)

a Asterisks indicate where instead of cell volume, the volume of a l-mm ﬁlament is given. b Bold ﬁgures indicate a typical middle-of-the-range value. Source: Developed from Reynolds (1998c).

objective. The mechanical aspects of artificial of stream was cleared of most of its detached mixing are reviewed in a later section (8.3.5). algae downstream of an abandoned straw bale, Mention may be made here of the use of theidea quickly spread that straw added to barley straw as a defence against Cyanobacteria. ponds and small reservoirs would provide effec- Fromachance observation in which a length tive protection from cyanobacterial growth. The ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 407 implicit confidence in the technique seemed mis- sition and local oxygen depletion. ‘Brown tides’ placed, as there was no information upon the of the picoplanktic Aureococcus and ‘green tides’ mechanism and the instances of successful treat- of Phaeocystis in its microplanktic colonial stages ments represented a very small proportion of may cause considerable distress among fisher- the attempts. By degrees, however, it became men. It has become fashionable to lump all these clear that the effective agent was a phenolic organisms together as ‘harmful algae’; certainly, substance, presumably produced by the barley they are the subjects of several recent reviews and plant (as in other plants, including bark-bearing compendia (see e.g. Anderson et al., 1998;Reguera woody plants) as a live defence against fungi et al., 1998). and microorganisms. It is released from the However, the particular issue of the red- straw as itagesandrots and the substance will tide dinoflagellates remains an intriguing one. A inhibit growth in the laboratory of Cyanobac- dozen or so genera are known to produce low- teria and other algae at quite low concentra- molecular-weight saxitoxins which are acutely tions (Newman and Barrett, 1993). Suitably aged, neurotoxic to birds, fish and humans. Being endo- broken up and dispersed, barley straw has been toxins (that is, they are not released into the shown to be reliably effective in preventing the water by livecells), they are apparently far more growth of nuisance blue-green algae (Everall and injurious to larger organisms than to planktic Lees, 1996;Barrett et al., 1999). Although there assembalges. One well-known pathway leading to is inevitably some imprecision in what makes an human poisoning is through the consumption of effective dose and algae show some variation in filter-feeding shellfish taken from areas recently susceptibility to barley toxins, the use of straw affected by red-tide organisms. should be recognised as a legitimate and effective The development of significant concentra- defence against Cyanobacteria, capable of induc- tions of relevant dinoflagellates is, in part, ing species-specific algal mortalities and altering attributable to high local nutrient inputs. Over dominance in mixed assemblages (Brownlee et al., the last three decades or so, red-tide events and 2003). The comment is still inspired, however, their constituent organisms have been becoming that the use of a toxic agent to protect against more frequent in the enriched coastal and shelf another toxic agent is faintly ironic, although, as waters adjacent to major urban centres of the already admitted, there may be other reasons for world (north-west Europe’s Atlantic seaboard, the seeking to eradicate Cyanobacteria from ponds St Lawrence, the Gulfs of Maine and of Mexico, and reservoirs. off Baja California, the north-eastern seaboard of Argentina, around Japan and Korea, and Aus- Red tides tralia and New Zealand). However, abundance is Several phyletic groups of marine phytoplankton compounded locally by the ability of the algae to have toxic representatives. Besides the dinoflag- self-regulate in slack water and to become aggre- ellates mentioned at the start of Section 8.3.2, gatedbyweak water movements. Thus, the devel- they include a handful of haptophyte genera opment of red tides is substantially consequent (mainly especially the Prymnesiales) that pro- upon the containment of populations by near- duce substances causing osmoregulatory failure surface stratification of enriched waters, or in and death in fish. Both Prymnesium parvum and shallow water columns (Smayda, 2002). Chrysochromulina polylepis have been implicated in It seems that the natural habitats and prob- fish kills around the North Sea coast, the alga able sources of many of the more troublesome having first built unusually large local popula- of the red-tide species are associated with the tions in each instance (see, for instance, Edvard- exploitation of rapid nutrient renewal in frontal sen and Paasche, 1998). In addition, non-toxic zones and post-upwelling relaxations, where species have been implicated in fish kills as reduced mixing and relative resource abundance a consequence of local algal abundance, near- normally coincide (see Figs. 7.3, 7.4 and Section simultaneous death, followed by rapid decompo- 7.2.2). Alexandrium tamarense and Karenia mikimotoi 408 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

8.3.3 Controlling eutrophication by phosphorus load reduction The worth of the Vollenweider–OECD regression lies in the elegant empirical statement it makes about the generalised behaviour of the lakes included in the original dataset upon which it is based. It makes no statement about any individual lake, beyond the qualitative deduction that if it becomes more enriched, it may well sup- Figure 8.6 (a) Selection trajectory in the sea, as proposed port more phytoplankton chlorophyll on average. by Smayda and Reynolds (2001), accepting that more of the Still less does it confirm that reducing current potential resource/processing interaction is inhospitable to phosphorus loads will result in the support of phytoplankton. The trajectory now closely resembles more modest algal populations. Yet many man- Margalef’s ‘main sequence’ (see Fig. 7.2). (b) By analogy, the agers have been deceived by the power of the ‘red-tide sequence’ (here styled HAB sequence) runs parallel regression to employ it as a driver and measure to the main sequence but more deeply into environments made more tenable by greater nutrients and reduced depth of of schemes intended to reverse eutrophication mixing, representing the involvement of bloom-forming taxa and restore the lake to something supposed to be in the active community. Redrawn with permission from closer to ‘pristine’ conditions. This latter, rather Smayda and Reynolds (2001). nebulously used, term usually refers to a state that preceded the agricultural–industrial anthropogenic impacts and not to the conditions at the lake’s birth. Even so, the Vollenweider–OECD rela- are typical members of the frontal flora in mid- tionship is not a management tool, nor was it dle latitudes, while Lingulodinium polyedrum and ever intended as such. It may be seen as a guide Gymnodinium catenatum are notable toxic species to thedetermination of nutrient loads and to of upwelling relaxations. The highly toxic Pyro- theprospects for the benefits to be gained from dinium bahamense and Karenia brevis are adapted to their reduction. It is ‘not a slope, up or down entrainment and dispersal in offshore currents. which a given lake will progress during a period The links among size and morphology (life of artificial enrichment or deliberate restoration’ form), physiology and ecology that have been (Reynolds, 1992a,p.5). noted at frequent intervals in this book were On the other hand, some restoration schemes, explored famously by Margalef (1978), and not involving the alleviation of anthropogenic phos- least in the context of an early exposition of the phorus loads, either by diversion or tertiary treat- causes of red tides (Margalef et al., 1979). In their ment of the sewage inflows, have been spec- mandala (Fig. 7.2), the ‘red-tide sequence’ was tacularly successful. One of the best-known and represented as a sort of system ‘sickness’, strik- most-cited examples concerns the abrupt reducing parallel to the successional ‘main sequence’, tions in the average phytoplankton biomass in in an area of greater nutrient availability. In Lake Washington, in the north-west USA, fol- the context of the C–S–R triangle, preferred by lowing the diversion of all sewage discharges Smayda and Reynolds (2001), increased nutrient to the lake. Once the diversions began to take enrichment of coastal waters permits a higher effect, from the mid-1960s, the phytoplankton arc than the main sequence to be traced (Fig. biomass, for long dominated year-round by Plank- 8.6). This is more favourable to the Type-IV, Type-V tothrix agardhii,was quickly reduced to below or Type-VI species associations than to the glean- its 1933 level (the first year for which quanti- ing, K-selected S-strategists normally culminating taive records had been kept) (Edmondson, 1970, Margalef’s (1978)mainsequence.However, Fig. 8.6 1972). By 1976, the alga had effectively disap- gives little new insight into why these species peared, leaving microplankters dominating the should be toxic or what benefit obtains. This reduced phytoplankton biomass, and average explanation is still sought. Secchi-disk transparency cleared from <2mto ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 409

Figure 8.7 Stages in the recovery of three European lakes the editorship of H. Sas (1989), showed substantial after reduction in external phosphorus loading. Heavy lines differences in their responses to reduced external link the changing observed annual average chlorophyll a Ploads, most especially between lakes judged to concentrations against the phosphorus availability and are be ‘deep’ and those considered as ‘shallow’. There superimposed upon the slope of the Vollenweider–OECD were also systematic differences in the onset of regression. The bars to the right of each point represent the the biological response to the diminished deliv- difference between TP (total phosphorus) and PP (the ery of phosphorus to the lake (Sas’ Subsystem 1) particulate fraction). Note that the difference, approximately which was consistently mediated through the equivalent to unused dissolved P, is virtually exhausted before there is a response in the mean chlorophyll concentration. bioavailability to algal production (Subsystem 2). Redrawn with permission from Reynolds (1992a). Three cases are illustrated in Fig. 8.7. The first concerns the Wahnbach Talsperre, a mainstem reservoir on the River Sieg that sup- >4m.Furtherconsequential changes included plies water to Bonn and Koln¨ in Germany. During the riseofDaphnia species and their replace- theearly 1970s, unacceptably large, year-round ment of Diaphanosoma and Leptodiatomus as domi- crops of Planktothrix rubescens were proving expen- nant zooplankters, with further benefits to water sive to treat for potability. The morphology of the clarity (Edmondson and Litt, 1982). Other asso- valley in the inflow region lent itself to the con- ciated changes in the structure of the plank- struction of a small pre-reservoir and a treatment tic food web have been consistent with the lake plant that would remove biogenic debris, partic- recovering an essentially mesotrophic condition ulate matter and dissolved phosphorus from the (Edmondson and Lehman, 1981). inflow, so that the water in the reservoir was The Lake Washington case has been an endur- rendered much less supportive of phytoplankton ing example of what can be achieved when the growth. This approach to tackling the problem of eutrophication is still relatively mild (Lorenzen, diffuse phosphorus loads was novel, costly and, 1974). Schemes elsewhere have not necessarily so far, scarcely imitated, but the savings in water been quite so successful, either taking long peri- treatment and disinfection for distribution have ods totakeeffector,insomecases,havingstill repaid the investment. However, there was some to show improvements (Marsden, 1989). The need nervousness in the early days following commis- to understand these apparently quite different sioning, for although the dominance of Plankto- sensitivities of lakes to altered phosphorus loads thrix waseroded, diatom blooms became more provided the inspiration for the analysis carried prominent in the phytoplankton and these were out by Instituut voor Milieu- en Systeem-Analyse still disappointingly expensive to treat (Clasen, (IMSA) in Amsterdam. The study, published under 1979). Eventually though, as Subsystem 2 in-lake 410 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

Figure 8.8 (a) Revised explanation of lake responses to halved between 1975 and 1979 but with lit- phosphorus-load reductions, including changes in tle effect either upon the average phytoplank- phytoplankton composition. Reading from right to left ton biomass or its species composition. A steep approximates the effects of eutrophication. (b) Hypothetical P–chl relationships for individual lakes. The fitting of an decline in the phytoplankton mass occurred in averaged regression probably underestimates the slope of chl theearly 1980s, once the available phosphorus a on P in those lakes where it is genuinely a limiting constraint had been lowered to a point below the demand on biomass-carrying capacity Redrawn with permission from of previous maximum crops, MRP had become Reynolds (1992a). acrop-limiting resource. Again, the slope of response was close to 1 : 1 and steeper than Vol- lenweider mean. In Schlachtensee (Fig. 8.7c), the phosphorus availability slowly adjusted to the lag between the sharp reduction in phosphorus sharp depletion in subsystem 1 phosphorus deliv- loading between 1981 and 1984 (when bioavail- ery, so annual average chlorophyll concentrations ability was also reduced eight- to tenfold) and also declined. By 1985, the reservoir had achieved any noticeable impact upon average phytoplank- an oligotrophic status (Fig. 8.7a). Of particular toncrops was plainly related to the prior diminu- interest is that the line fitted to the year-on-year tion of the large cushion of unused MRP. Once averages is rather steeper than the Vollenwei- again, the eventual, near-linear biomass response der OECD regression. It is in fact almost linear, depended upon the prior imposition of a demon- at 1 : 1, reflecting the fact that phosphorus had strable capacity limitation by the bioavailable become the capacity-controlling resource and, so, phosphorus. Without that, biomass is insensitive truly limiting to phytoplankton crops supported. to the actual amounts of phosphorus supplied to In Veluwemeer (Fig. 8.7b), one of the polder its growth medium. lakes bordering the reclaimed Ijssel Meer, prob- The behaviours represented in Fig. 8.7 are lems of excessive Planktothrix agardhii growth generic. The general case, proposed in Sas (1989) were addressed by interception of the main point and reproduced in Fig. 8.8a, has received wide sources of phosphorus and by progressive flush- acceptance. Reducing phosphorus loads have lit- ing with a more dilute water source (Hosper, tle effect on biomass while unused PP capacity 1984). In-lake TP concentrations, then about ten saturates the requirements of the biomass suf- times those in the Wahnbach Talsperre, were fering some other constraint. Movement from ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 411 stage 1 to a P-led biomass reduction (stage 3) gate of the MRP load and which is broadly pre- and a switch, perhaps, away from relative abun- dictable (Eq. 8.3,Section 8.3.1 above). Its trans- dance of Cyanobacteria to (e.g.) more benign fertobiomass alters the MRP concentration in chlorophyte–chrysophyte associations (stage 4) thewater but – theoretically – without alter- depends upon the reduction in P availability to ation to the TP content of the water and with- apointwhen it imposes the main constraint out affecting its overall bioavailability (though on biomass carrying capacity. The critical quan- it is temporarily restricted to those organisms tities are unique to each individual lake, how- that took it up). The subsequent fate of the par- ever, so the coordinates of the response curve are ticulate P (and the organismic P in particular) lake-specific. It is not difficult to recognise that does very much affect its future bioavailability theVollenweider–OECD regression is actually fit- and to whom. Whether the first beneficiary is tedtowhat are ultimately the biomass response eaten and its phosphorus incorporated in the curves to P loads for the individual lakes (notion- biomass of the consumer, or its cadavers are bac- ally shown in Fig. 8.8b). Then, the more lakes terised and the phosphorus is recycled to the that are featured in which the phytoplankton water, theeffect of the intervention of the food biomass is not severely or continuously P-limited, webistwofold. Either phosphorus ends up in the then the flatter would be the fitted slope. The biomass of large organisms (macrophytes, fish, Vollenweider–OECD coefficient of 0.91 reflects a birds, mammals), whence it is possibly exported higher representation of P-deficient oligotrophic from the lake, or it contributes to a flux of bio- lakes in the original dataset than (say) among the genic deposits. Typically, these products range (mainly) North American lakes analysed by Rast from plant necromass (wood, rhizomes, leaves, and Lee (1978)toyieldacoefficient of 0.76. consigned to slow, microaerophilous decay) to In the context of controlling Cyanobacteria, therain of fine planktogenic detritus that set- the analysisofsiterestorations considered by tles down towards the bottom of the lake. On Sas (1989)unexpectedly revealed another com- geochemical scales, such sedimentary phospho- mon behavioral feature. Before any noticeable rusmay eventually be liberated but, in ecolog- biomass or compositional response to reduced ical terms, the possibilities for its release and in-lake P availability had occurred, several of reuse are strikingly habitat-dependent. Biogenic the lakes with large or dominant component of organic materials reaching the bottom of the bloom-forming Cyanobacteria showed a consid- water column contain still-reduced carbon and erable increase in clarity (actually, Secchi-disk avariety of other co-associated elements (includ- transparency). This observation was explained ing phosphorus). These become the resource of by a deeper average vertical distribution of the benthic food webs in which detritivorous and Cyanobacteria and other self-regulating species. decomposer organisms assemble and maintain The expectation that average buoyancy in gas- their respective biomass and perhaps sustain the vacuolate Cyanobacteria should respond to low- assembly of benthic consumers (including fish). ered ambient nutrient concentrations (see p. Collectively, the potential effect of the benthic 206), thereby permitting the algae to scour for food web is progressively to oxidise the carbon resources more deeply in the water column, is and to liberate the other elements which steadily strongly upheld by these observations. Sas (1989) become in stoichiometric excess. included this behavioural response in the generic The influence of habitat on this process oper- curve (Fig. 8.8a) as a discrete stage 2. ates first through depth. As has been pointed It remains to explore the between-site differ- out earlier (Section 8.2.3), much of the pelagic ences in the Subsystem 1 – Subsystem 2 linkage sedimentary output in the sea is oxidised and and the difficulty, or otherwise, of depriving phy- its more labile associated nutrients (including toplankton of sufficient bioavailable phosphorus nitrates and phosphate) are liberated within 200 for themtocontinue to grow and replicate. The mofthe surface. Nutrient cycling is not nec- potential unexploited BAP concentration has a essarily impaired in lakes substantially <200 m direct, steady-state relationship with the aggre- in depth, although the largely diffusive return 412 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

pathways, even for the most soluble nitrogenous through its combination with excess sulphide components, operate more slowly than in the ions (which are liberated by sulphate reduction open turbulence of the water column. The supply under slightly lower redox levels than required of oxidant can also become problematic, insofar foroxidation of the ferrous ion) and preciptated as annual net organic carbon fluxes of >100 mg as FeS, then the potential for chemical scaveng- Cm−2 carry an oxidative demand that may well ing of phosphate by ferric iron during the next challenge the capacity of the ‘deep sediments’ oxidation is proportionately weaker. Accordingly, (in this conext, anywhere between about 5 and more phosphate will be available to biotic recyc- 200 m from the surface) to satisfy, especially in ling. periods of density stratification. Indeed, beneath What emerges is that in a majority of lakes an oxidised microzone, the sediments and their of less than 200 m in depth, the bottom sedi- interstitial liquor is anaerobic and strongly reduc- ments normally function as a phosphorus sink. ing. Carbon oxidation and nutrient release are Phosphorus atoms take a single, albeit devious, correspondingly slow, ecological function being trip from hydrological catchment to permanent truly ‘oxidant limited’ (also as discussed in Sec- lake sediment. Tomorrow’s production effectively tion 8.2.3 and represented in Fig. 8.2). With still depends upon tomorrow’s (or even today’s) deliv- greater contributions of organic carbon from the ery of external phosphorus. Were this not so, nei- production of eutrophic lakes, the oxygen deficit ther the Vollenweider model nor the restoration may extend well into the hypolimnetic water methods that rest upon its central philosophy above the bottom sediment, where the rate of can work. It is the mechanism by which trunca- its biological reuse and organic decomposition is tion of the external phosphorus load to the water equally depressed. column results directly lowered phytoplankton- Against the background of differential oxida- supportive capacity. The new steady-state can tive turbulent entrainment rates, the recycling be struck, usually within two to three reten- of phosphorus becomes similarly varied (see e.g. tion times (Ryding and Rast, 1989;Reynolds Reynolds and Davies, 2001). Orthophosphate ions and Irish, 2000). The limiting condition to this released from decomposing biomass into the statement is the saturation of the phosphorus- interstitial water of oxidised superficial sedi- binding capacity of the sediment iron, either by ments may travel but a short distance before excessive orthophosphate recruitment or by the being exchanged preferentially for hydroxyls on onset of high alkalinities (caused, for instance, thesurface of iron flocs and clay minerals in the by episodes of high productivity, carbon with- sediment (Reynolds and Davies, 2001). Here, they drawal and base generation). With eutrophica- are effectively immobilised, pending the onset of tion comes the prospect of accelerated recruit- strongly reducing conditions (in which the fer- ment to sediments, possible saturation of the P- ric ion Fe3+ ion is reduced, biotically and abi- binding capacity and its complete suppression otically, to the soluble ferrous Fe2+ ion; see Sec- by anoxic reducing conditions. Even then, the tion 4.3.1)orincreased alkalinity, in which excess deeper sediments do not give up orthophosphate hydroxyls now displace immobilised phosphate to thewater column very readily and little is nec- ions. Though potentially bioavailable in this form essarily returned to the water column for biotic (Golterman et al., 1969), phosphate thus liberated reuse and recycling. into the interstitial of anaerobic sediments (or equally, into the anaerobic hypolimnetic water if 8.3.4 The internal load problem present) is likely to be once again scavenged and As noted by Sas (1989), the further contribu- immobilised by iron reprecipitating on exposure tory process which so delays the restoration of to oxygen. This is important, because the act of eutrophied shallow lakes is that the phosphorus- re-solution of iron-bound phosphate is not ‘recy- rich interstitial water is much more readily re- cled’ to the biota if it is just re-precipitated in entrained than it ever is from deep sediments the non-bioavailable form. If, in the interim, the protected by adjacent boundary layers. Struc- mass of reduced iron is diminished, for instance tural disruption of the shallow deposits, mostly ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 413 through their physical penetration by wind- or municipal investment in P reduction had failed wave-driven turbulence currents, may well result to ameliorate the eutrophication of the shal- in the discharge of interstitial water and its low lake Trummen, in Sweden, and nothing less solutes into the main water column. Applied to than the dredging and removal of the veneer fine superficial sediments, turbulent shear, dissi- of P-saturated sediment was needed in order to pating energy at rates in the range, E = 10−6 to restore an acceptable quality to the lake (Bjork,¨ 10−5 m2 s−3 (see Table 2.2 and Section 2.3.4), is 1972, 1988). This is an expensive, disruptive and capable of penetrating and resuspending mate- problematic technique, not least because of the rial from a thickness 30–40 mm (Nixon, 1988). high water content and fluidity of the dredged or The process can be abetted through the activities air-lifted material. In spite of its potential fertil- of burrowing animals and foraging fish (‘bioturb- ity as a soil conditioner, the material is not eas- ation’; see, for instance, Davis et al., 1975;Petr, ily stored and de-watered except on level ground. 1977). The kinetics of ‘phosphorus release’ from Notsurprisingly, lake restoration based upon sed- the sediments to the water have been the sub- iment removal has been little practised. ject of several major overviews (including Kamp- There is, however, considerable interest in Nielsen, 1975;Baccini, 1985;Bostrom¨ et al., 1988). arecent methodological development involving Ultimately, however, it is the relative scarcity theapplication of clay minerals to shallow water of significant chemical binding capacity in the bodies prone to free cycling of phosphorus (Dou- water that permits the phosphorus thus released glas et al., 1998). These imitate the P-binding prop- to become once again substantially bioavailable erties of metal oxides and hydroxides but with- to planktic producers. out causing the toxicity problems that direct dos- The further deduction that can be made is ing of (say) iron or alum salts might cause to that, whereas deep lakes are likely to respond to water bodies. The binding performance of mod- (i.e. be sensitive to) managed reductions in nutri- ified clay minerals based on lanthanum is espe- ent loads, the prospect for successful restora- cially effective, removing phosphorus from solution of eutrophied small shallow lakes is prob- tion and firmly immobilising it in the particulate ably much poorer after they have once been sedimentary fraction. enriched significantly. The greater likelihood is As the techniques for treating and restoring that historic phosphorus loads will, on ecologi- lakes through nutrient reduction become more cal scales, thereafter be recycled indefinitely (van varied in concept and suitability, it becomes der Molen and Boers, 1994). A case in point is that increasingly important to managers to seek guid- of Søbygaard, a highly eutrophied shallow lake in ance in selecting the most effective approach and Denmark, where a sixfold reduction in the exter- to predict its prospects of success. Such knowl- nal phosphorus load of ∼30 g P m−2 a−1 had not edge might also assist the prioritisation of invest- succeeded, even after 12 years, in reducing MRP ment among competing schemes of restoration. levels in the lake to anywhere near a point where What is required is a simple basis for distin- they might limit phytoplankton biomass capac- guishing among the sites where, to use the ter- ity in the lake (Søndergaard et al., 1993;Jeppe- minology of Carpenter et al.(1999), eutrophica- sen et al., 1998). By analogy, efforts to reduce tion is either readily reversible (response immedi- external phosphorus loads on large, shallow Lake ate and in proportion to the change in P load- Okeechobee, Florida, USA, have so far failed to ing), hysteretic (requiring profound reductions in bring about restorative changes in the ecology Pinput over a protracted time period) or irre- of the lake, which continues to function on the versible (recovery impossible by reducing P inputs support lent by internal P cycles (Havens et al., alone). As indicated in the IMSA study (see Sas, 1996). 1989,above),themostsensitive direct measure The available data make plain that mas- of the sensitivity of the biomass to change is the sive P recycling continues to be maintained amount of bioavailable P capacity in Subsystem quite independently of present external loadings. 2that remains outside the biomass. This ‘cush- In another much-cited instance, a considerable ion’ then represents the hysteretic resistance to 414 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

change that must be all but exhausted before Plainly, the lower the product, the more the biomass is made dependent upon altered loads. lake is expected to respond to altered P loads. Sensitivity is then reduced to the latitude of Reynolds (2003c)also proposed a further factor TP–MRP transformation and the extent to which to cover the importance of good water quality internal recycling of MRP is suppressed by sedi- at the particular site (internationally important ment binding. amenity, drinking-water source, local wildlife Following on from an earlier attempt reserve, etc.). It was urged that the total product (Reynolds et al., 1998)tocategorise the rela- should not determine prioritisation for corrective dependence of biomass to each of a num- tive treatment but rather prompt further inves- ber of environmental variables, Reynolds (2003c) tigation of the importance of overcoming high used the inferred phosphorus thresholds to factors; nevertheless, it was noted that low over- inform a sensitivity model. This involved scoring all scores (≤6) would refer to high-quality sites against each of a number of categories (trophic whose trophic state should be ruthlesly defended, state, hydraulic retention, bicarbonate availabil- whereas scores up to 32 are indicative of sites ity and the extent of shallow sediments likely to that should respond hysteretically to altered exchange phosphorus). The lower the score value, nutrient loads. Sites with higher scores may err the greater is the sensitivity to change. beyond the bounds of a likely reversal of eutroph- The first of these took the five trophic divi- ication. sions in Table 8.1. Where small amounts of The UK Environment Agency now uses a phosphorus are available, dependency is high scheme, based upon this approach, to assist the and, accordingly, small changes in P loading implementation of its Eutrophication Strategy. will invoke significant responses; thus ultraoligotrophic lakes score 1, hypertrophic 5. Flush- 8.3.5 Physical methods to control ing lowers the responsiveness to nutrients; thus, phytoplankton abundance lakes were considered to be sensitive (1) to P-load Alternative practical approaches to the control of variation if the hydraulic retention time (tq)was phytoplankton biomass yield, the rate of capacity >30 d, not at all so (3) if tq <3dand slightly attainment and, in many instances, its species so (2) when 3 d < tq <30 d. Bicarbonate alkalin- composition have invoked the artificial enhance- ity and the elevated frequency of opportunities ment of the physical processing constraints. for phosphorus exchanges at high pH also affect Methods for extending the period of full arti- sensitivity and this is reflected in the grading of ficial mixing in lakes deep enough to stratify, alkalinity. Lakes are sensitive (1) where bicarbon- either by artificial destratification or by prevent- ate alkalinity <0.4 meq L−1,notat all sensitive ing the onset of stratification at all. The princi- (3) to alkalinities >2meqL−1,and slightly sen- ple that is invoked is the one illustrated in Fig. sitive (2) when 0.4 < alkalinity < 2.0 meq L−1. 3.19,wherethegreater is the depth of the layer Similarly, recognising the propensity for shallow- in which algae are entrained, then the greater is water recycling, water bodies are considered to be thedilution of the light-determined supportive sensitive (1) to changes in external load if <15% capacity. It is not just that the algae (say, at an of the surface covered sediments <5mdeepbut areal concentration of 80 mg chla m−2)maybe insensitive (3) if >50% of the lake is shallower diluted from a high near-surface concentration than 5 m; lakes where >15% but <50% is under (80 mg chla m−3,ifconfined to the top metre) to 5mdeep are considered to be slightly sensi- being spread uniformly through the top 80 m, at tive (2). Multiplication of the four factors yields a concentration of 1 mg chla m−3,buttheplot aproduct between 1 (a deep, ultraoligotrophic says this is the maximum concentration that an lake with a chronically low phosphorus con- 80- m mixed layer could possibly support, as cal- tent, low alkalinity and long retention) and 135 culated according to Eq. (3.25)inSection 3.5.3 (for a shallow hypertrophic river fed pool, sub- and assuming the most favourable conditions of ject to rapid flushing by nutrient rich calcreous insolation (I0) and background absorption (εw + flow). εp). Mixed through only 40 m, the maximum ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 415 supportable concentration is closer to 20 mg chla This also requires energy expenditure and, thus, m−3 (i.e. 800 mg chla m−2). Mixed through 10 an appropriate cost–benefit analysis; the benefits m, the maximum supportable concentration is may include the direct effects of aeration, as well about 160 mg chla m−3 (or 1600 mg chla m−2). as mixing. Yet another method is to force the Using this logic in reverse, increasing the depth inflow through angled nozzles that direct the jets of mixing ameliorates the concentration of algae of water to maximise their homogenising effect in the reservoir water to be treated for potabil- (Toms, 1987). ity, especially if the water is at all coloured or Caution is urged, however, against an assump- carries a significant non-algal turbidity. The sev- tion that lack of stratification is necessarily eral Thames Valley storage reservoirs that serve indicative of being well mixed. My experience London have either been subjected to artificial from several reservoirs where pumps or bubble mixing (Ridley, 1970;Steel,1972, 1975)orthey plumes are in operation agrees with the view have been commissioned since that time with the that temperature gradients are generally weak, capability built in at the design stage (Steel and or non-existent in the immediate environs of the Duncan, 1999). The benefits, in terms of filtration device. Further away, phytoplankton may still be efficiency and savings on the cost of treatment, disentrained and the self-regulating species may have been substantial and worthwhile and the perhaps engineer slightly better growth condi- nuisance Cyanobacteria are scarcely represented tions for themselves. It may be sufficient just to any longer in the planktic flora of the reser- keep stratification weak, so that the work of wind voirs inoperation (Toms, 1987;SteelandDuncan, and cooling can more easily mix the water col- 1999). umn from time to time. Modelling algal growth The methods for overcoming and prevent- in reservoirs with PROTECH (Section 5.5.5;work ing thermal stratification and for extending the still in process of publication at the time of period of non-stratification have been in use this book going to press) has strongly suggested for many years and are well established (Irwin to me that many such reservoirs are often less et al., 1969; Dunst et al., 1974;Tolland, 1977; well mixed than supposed. On the other hand, Simmons, 1998;Kirke,2000). The most success- other reservoirs without any other source of arti- ful of these function as lift pumps, comprising ficial mixing also remain very weakly stratified, avertical cylinder with either a paddle or a at those times when water is drawn off for treat- injected bubble stream todrawcolddeep water ment from near the bottom of the water column. to within a short distance from the surface where Unless it is unsatisfactory on chemical or biolog- the flow diffuses laterally. Another device, the ical grounds, I believe it to be preferable to draw Helixor®,usesanArchimedeanscrewtoachieve waterfrom depth as it yields water of reason- asimilar effect. By setting up entraining vor- able quality but (literally) undermines the ten- tices, these devices move rather more water than dency to stratify. The power-generating plant sit- flows through the cylinders. Moreover, they work uated at the dam of Brasil’s Volta Grande Reser- reasonably efficiently so long as water is dis- voir draws its flow from the base of the reser- charged from the pipe below the surface of the voir and, in complete contrast to others in the water body: lifting water above the surface level cascade, fails to stratify (Reynolds, 1987b). A 70- requires a rather greater pumping effort. Most m, near-isothermal water column in a tropical use electrical power to drive the pumps (the alter- impoundment is an unforgettable surprise to a native is wind power) and their operation car- limnologist! ries significant costs, which have to be balanced The phytoplankton in this reservoir also dif- against the savings to be made on treatment and fered fromthat of others in the chain. The disinfection. unstable water column of Volta Grande was Another popular method of weakening strati- dominated by the diatom Aulacoseira and the fication is to use bubble plumes: punctured hose desmid Staurastrum,together constituting an or tubing is laid out on the reservoir floor and assemblage classifiable as Association P. This is compressed air is forced out of the perforations. one of the groups of mainly R-strategist groups 416 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

whose natural occurrence is in well-mixed water nique of directly applying powdered copper sul- columns and whose ascendency can be stim- phate to reservoirs as an algicide. The salt dis- ulated in lakes and reservoirs by episodes of solves easily in the water, where a strength of 1 artificial or experimental mixing (Lund, 1971; mg L−1 of the penthydrate is sufficient to kill Reynolds et al., 1983b, 1984;Reynolds, 1986b). most species of phytoplankton and – inciden- Restratification may revert the flora to species tally – more than enough to administer a lethal either less dependent upon entrainment for sus- dose to crustacean zooplankters (my own unpub- pension or more dependent upon disentrain- lished observations). The effectiveness of the ment to have any chance of harvesting suffi- treatment against algae seemed to vary, appar- cient light (i.e. C-strategist nanoplankton and ently in relation to the degree of mucilage invest- motile microplankton, including the larger, self- ment (Coesel, 1994;see also Box 6.1, p. 273). Most regulating S-strategist species). The possibility of of the copper is eventually precipitated and sinks alternating conditions, before any particular set to thesediment. Therein resides the problem, of adaptations led one group of species to become forthe copper remains sensitive to changes in overabundant, was specifically investigated in the acidity and redox potential. The salutary case of study of Reynolds et al.(1984)and through the thegross copper poisoning of the Fairmont Lakes population dynamics of selected algal respon- Reservoir, Minnesota, USA, following years of fre- dents (Reynolds, 1983a, 1983b, 1984c). This led quent dosing to control algal growths (Hanson Reynolds to propose an approach to manag- and Stefan, 1984) both confirmed the worst fears ing reservoirs by mixing them intermittently, about the potential threats of long-term copper in order to prevent any group becoming too applications and doubtless influenced the ban- numerous. Reynolds et al.(1984) conceded that ning of its use in many countries. it was probably too cumbersome to apply safely, in the sense of maintaining close control over 8.3.6 The control of phytoplankton by phytoplankton biomass. Generally (and always biological manipulation provided that the water column is sufficiently As an alternative to being able to control ade- deep and/or the water sufficiently turbid), per- quately the biomass-supportive capacity, the idea sistent mixing to control light-determined carry- of regulating its allocation among desirable and ing capacity is the simpler and more efficient undesirable biota has had a long-standing appeal option. However, a potential drawback of doing in lake management. The term ‘biomanipula- this, which was of concern to Lund (1971, 1975; tion’, coined originally by Shapiro et al.(1975), Lund and Reynolds, 1982), is that prolonged mix- has become increasingly restricted to refer to the ing would lead surely and ultimately to domi- control of undesired organisms by the deliberate nance by such organisms from functional group adjustment of the abundance of the next trophic S1.Onceestablished, prevalence of Planktothrix level of consumers. The underpinning logic is agardhii, Limnothrix redekei or Pseudanabaena lim- thesame one that distinguishes ‘bottom–up’ netica is hard to overcome (Reynolds, 1989b). That from top–down processes (see pp. 287--8). Thus, this has not happened in the case of the routinely not surprisingly, it has been just as controver- destratified Thames Valley reservoirs seems to be sial and contested just as vehemently (see, for a function of their short retention times (usu- instance, Carpenter and Kitchell, 1992;DeMelo ally <20 days) (Toms, 1987;Reynolds, 1993b). The et al., 1992). However, also like the ‘bottom–up combination of a hydrological displacement time vs. top–down’ debate, the issues ceased to be of just 10–30 days and a fairly intensive mixing so contentious, once the critical roles of vari- regime is perhaps decisive in the continued ability and site-specific factors affecting resource exclusion of Planktothrix. turnover became more clearly understood. There Mention of the treatment orpreventionof is, for instance, a much wider acceptance algal growth in drinking water reservoirs gives an of the importance of the basic carbon path- appropriate opportunity to refer briefly to once- ways in determining the optimum functional common practice but now much discredited tech- adaptations and, so, the identity of the most ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 417 efficient traits (discussion in Sections 8.2.3 and trophogenic layer of the water column and its 8.2.4). Interestingly, the assumption of direct periodic exposure to the shear stress of the suface and manipulable linkages between phytoplank- mixed layer. This property influences both the ton, zooplankton, planktivorous fish and pisci- cycling of resources and the interactions between vores is now argued to provide an acceptable benthic and planktic consumers. However, the model only for truly pelagic systems. To apply remarks apply broadly to lakes in which >50% thedeductive reasoning that says (e.g.) the selec- of the area is shallower than 5 m (as in Section tive removal ofpiscivoresdistortsthefoodwebby 8.3.4). sparing planktivorous fish to prey more heavily The supportive capacity of shallow lakes may on zooplankton and promote a larger phytoplank- be regulated by hydraulic throughput, turbidity ton biomass, requires effective management over or colour but, naturally, the supply and chem- very substantial areas of the pelagic. Similarly, ical binding of phosphorus are frequently such to approach the problem of phytoplankton over- to regulate the accumulation of biomass. Modest abundance fuelled by extra nutrients simply by depth and high perimeter to volume ratio, how- reducing planktivory or increasing piscivory in ever, leave the small water body quite vulnera- asmalllake is rather to ignore the role of the ble to drainage and the import of solutes and terrestrial subsidies and benthic feedbacks in particulates arising from land-use change, loss of undermining the system reliance upon phyto- vegetation, increased particulate loss from cul- plankton photosynthesis. Such retrospective con- tivated soil, as well as to incursion by any of a siderations aid the appreciation that the more large number of organic pollutants. With the pos- successful attempts to devise sustainable bioma- sible exception of chronically nutrient-deficient nipulative schemes for controlling phytoplank- small lakes, many are susceptible to quite rapid ton and attaining an aesthetically pleasing water ecological change – between clarity and high clarity have been most successful in small, shal- algal turbidity and between supporting exten- low lakes and ponds and least so in larger, deeper sive macrophytic vegetation, both submerged and lakes (Reynolds, 1994c). It is nevertheless neces- emergent. These fluctuations among periodically sary to qualify this statement again by saying steady states have been studied for some time that ‘if to biomanipulate is simply to distort the (Scheffer, 1989;Blindow et al., 1993;Scheffer et al., food chain simply attain a more beneficial con- 1993;Carpenter, 2001). Some of these transitions dition, then there is no theoretical objection to have now been empirically characterised and the biomanipulating an area the size of the Atlantic outcomes are helpful in informing strategies for Ocean’ (Reynolds, 1997a). If, however, the intent is securing the successful biomanipulative manage- an alternative, stable and self-sustaining system ment of shallow lakes. The following subsections but running on, broadly, the existing resource recount these. and energy inputs, then attention has to be given to the means of substituting alternative sys- Nutrients, phytoplankton and grazers tem components that process those inputs along There is no fundamental difference between quite different pathways. These alternatives are large and small lakes in the supportive capacity confined to small or shallow systems. Biomanip- of plant nutrients so the relationship between ulation of the functional importance of phyto- thepotential yield of phytoplankton chlorophyll plankton is a practical and sustainable corrective and the supportive capacity of bioavailable phos- to thesymptoms of eutrophication only in such phorus (as suggested in Eq. 4.15, Section 4.3.4) is water bodies. independent of lake size. Scheffer’s (1998)analy- In the context of the present chapter, the sis of the average summer chlorophyll yields of adjective ‘shallow’ is used more in its func- 88 shallow Dutch lakes, showing a slope close to tional sense than within any absolute constraint 1 µgchla (µgTP)−1 and saturating at about 300 (Padisak´ and Reynolds, 2003). The most impor- µgTPL−1 is in accord with expectation. Such con- tant property is the frequent or continuous concentrations of chlorophyll a are unexceptional tact of most of the bottom sediment with the in nutrient-rich shallow water, where they may 418 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

typically characterise near-unialgal populations to kept in check from its own potential growth of group-J or group-X1 chlorophytes or group-S1 and recruitment of filtration capacity (say 0.19 Planktotricheta (see Section 7.2.3). d−1), fish feeding needs to remove about 0.1 mg Whereas the latter may dominate perenni- zooplankton C L−1 d−1, but with rather narrow ally, the green algae may be subject to abrupt margins of variation. If we take the model of collapses, usually as a consequence of intensive Elliott and Hurley (2000a;see Section 8.2.2)and grazing by filter-feeding zooplankton, or, sub- estimate a requirement of 40 mg zooplankton C sequently, to recovery to large concentrations. per gram fresh-weight of fish per day, then the The dynamics of these fluctuations are best required stability would be struck when the fish known from systematic observations on com- biomass is equivalent to 1 g per 400 L or 2.5 mercially managed fishponds (Hrbacek´ et al., gfresh weight m−3.Noallowance is made in 1961;Hillbricht-Ilkowska and Weglenska, 1978; these approximations for variable temperature, Kor´ınek et al., 1987)butmanyhave been imitated day-to-day differences in phytoplankton growth in controlled experiments (Shapiro and Wright, potential or for the divorced timescale of changes 1984; Moss, 1990, 1992;Carpenter et al., 2001). in fish biomass, through progressive growth and Unchecked by consumers, phytoplankton can increasing appetites. grow to the limits of the supportive capacity Again, there is little encouragement here for (which may be set by light rather than by phos- realising a reliable and stable managed state. In phorus). Direct herbivorous consumers include one of the few really clear cases of an engineered rotifers and crustaceans and, at low latitudes, cer- stability among three trophic levels, Koˇr´ınek tain species of fish (Fernando, 1980;Nilssen,1984). et al.(1987)observed a persistent standing popu- Among temperate lakes, filter-feeding daphniids lation of cryptomonads, of 2–4 µgchla L−1 in prove to be well capable of developing biomass a carp pond. The check was exercised by an (equivalent to ∼1mgCL−1) (Section 8.2.3)with apparently steady population of Daphnia pulicaria, an aggregate filtration capacity (approaching numbering about 100 L−1.Carpwerepresent 1LL−1 d−1)that will overhaul the rate of algal but atanunspecifed ‘low level’. On restocking growth and rapidly clear the water of all fine with fish in the summer, there was, predictably, particulates. Without access to filterable foods, an abrupt decrease in Daphnia,followedbya the Daphnia quickly starve and thereismass rapid increase in chlorophyll a concentration, mortality among the smaller instars especially to >100 µgchla L−1. (Fig. 6.4). Filtration collapses, and the next phase of algal dominance can commence. This see-saw between alga and grazer mass is The role of macrophytes scarcely a management formula but the fluctu- This last example supports the conjectures about ations may well be damped in the presence of stability but it also reinforces the intuition that significant densities of young cyprinid fish. The heavy fish stocking is conducive to the over- expectation is that fish consumption of zooplank- abundance of phytoplankton in small lakes. On tonwill reduce the exploitation of the phyto- theother hand, the lurching, cyclical alterna- plankton yet still control it within acceptable lev- tion of bottom–up production and exploitative, els. The belief is that the persistence of high algal top–down responses is probably the norm in such populations is the consequence of overstocking highly managed systems. That similar behaviour with fish and the zooplankton is simply squeezed is not so apparent in less impacted systems, out. The truth is that even the three-component which may support fish production but without system is extremely difficult to balance. If a stable being subject to algal blooms of a consistency phytoplankton is desired, it needs to be cropped approaching that of pea soup, requires us to look as fast as it self-replicates. If it is able to dou- more closely at the trophic pathways in other ble once per day, then the zooplankton needs to types of small lake. Stability of water quality, at filter about half the water volume each day. If least at the time scales of season to season and, therequisite biomass (roughly 0.5 mg C L−1)is in many instances, from year to year, is usually ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 419 associated with a strong presence of macrophytic In this way, different types of macrophyte angiosperms and pteridophytes. tend to be associated with particular habitats. A Anumberoffamiliesisrepresented in the full spectrum of life forms may be encountered in aquatic macrophytic flora (for an up-to-date clear, oligotrophic lakes. Lobelia–Littorella stands account, see PokornýandKvet, 2003). All show develop offshore, where, simultaneously, the sed- secondary adaptations to one or other of the iments are sufficiently fine and the light pene- habits that they have adopted. These broadly sep- tration is good. Deeper and further out, dense arate among species that are either: rooted and stands of naiads and elodeids may develop, merg- fully submerged; rooted with emergent foliage; ing finally with the isoetids, the deepest-growing rooted with floating leaves; unrooted and float- macrophytes. Emergent flowering plants (reeds ing. Besides supplying one of its key needs in and reed-like plants such as Phragmites, Typha, abundance, water offers to submerged macro- Schoenoplectus and some associated herbs) may phytes the benefit of Archimedean support and develop on more silted shores, while stands of theequability of temperature fluctuation that fully submerged plants (such as Myriophyllum and surpasses that experienced by their terrestrial rel- Najas and various Potamogeton spp.) and plants atives. Aerating the submerged tissues (especially with floating leaves (nymphaeid water lilies) form theroots) was a major constraint to returning in front of them in quieter bays. In more enriched to water but itsachievementwasamajorevo- lowland lakes, the reedswamp may be prolific lutionary advance. The large interconnected air but the submerged plants are compressed into passages and the aerenchymatous tissue that dis- narrow depth ranges. In small, shallow ponds, a tinguish the structures of most aquatic species submerged vegetation of Myriophyllum or Cerato- are illustrative of the remarkable power of adap- phyllum may carpet the entire bottom. In clear, tation. Rooted macrophytes vie with microphytic calcareous shallows, the dominant plants may be algae for light and nutrients but it is plain that macroalgae – the stoneworts, such as Chara and they have inferior rates of growth and repli- Nitella. cation to autotrophic microorganisms. However, In their respective localities, macrophytes most macrophytes enjoy two crucial advantages may be regarded as ‘system engineers’ (Jones et over microalgae: through their roots, they have al., 1994), fulfilling a keystone role to many of access to nutrients in the sediments that are associated species (see Section 7.3.4). Dense plant not normally available to algae; and they are stands suppress turbulence and create a calm, able to develop tissues for the internal storage cryptic habitat to a trophic network of inverte- of excess photosynthetic products and reserves brates. It is an environment that traps fine silt of potentially limiting nutrients. Aquatic macro- and organic debris, whose deposition leads to phytes are able to colonise standing water in all atruncation of the water depth and a succes- climatic zones. Their distribution within lakes sion of swamp, marsh, and, finally, woodland is restricted to shallow water, to depths depend- species, whose centripetal invasion potentially ing mostly upon its clarity (the typical Secchi- obliterates open water (Tansley, 1939). The macro- disk reading is often a good guide to the lim- phytes or, more particularly, the fungal fragmen- its of colonisation by submerged plants; see Blin- tation and bacterial decomposition of seasonal dow, 1992). In clear, deep lakes, there is usually dieback, provide some direct source of nourish- avertical zonation of the principal species and ment to the community of benthic invertebrates life forms (PokornýandKv˘et, 2003). In the hor- but their primary role in the energy flow of the izontal, there may be many shores from which lake lies in the provision of habitat to many other they are excluded, for reasons to do with the producers. Surface-growing (epiphytic) algae and suitability of the substratum and its exposure fungi (together, the Aufwuchs) constitute a source to wind or wave action. Species also vary in the of food to snails, microcrustaceans and larval degrees of acidity or alkalinity they will tolerate, ephemeropterans. These have a variety of poten- and many are susceptible to changing levels of tial predators, including flatworms, hirudineans productivity. and beetles. Accumulating organic debris and 420 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

detritus is exploited by a variety of malacostra- This explanation is now widely accepted. It has cans and larval hemipterans and by dipterans, been supported by some direct measurements oligochaetes and bivalves. There is another layer of the light attenuation by epiphytes on eel- of predatory carnivores including larval odonates grass (Brush and Nixon, 2002). The critical photon and coleopterans. Macrophyte beds play host to a flux transmitted to the photosynthetic apparatus very complex web of trophic interactions. Ideally, to the host plant, before its own performance their part in the economy of the lake increases is impaired, will vary with its own depth and relatively and inversely to the size and depth thelevels of harvestable light. However, Brush of the lake. Quite plainly, in small or shallow and Nixon (2002)developed regressions predict- lakes, macrophyte beds are the focus of the most ing epiphyte densities of 10 mg dry mass per intense production and the location of most of cm2 reduced PAR transmission by 33–70%. This its producers. is slightly less than some of the values suggested in earlier studies. The nature and habit Effects of eutrophication on macrophytes of the epiphytes also influences light transmissi- In many instances of eutrophication of shal- bility: the biomass achieved by crustose growths low lakes, the first symptom of change has of naviculoid diatoms is less than what is attain- been the disruption and decline of macrophyte able by erect cells of Synedra-like diatoms or the dominance. Charophyte communities are con- branching arbuscular formations of Gomphonema sidered to be the most susceptible to replace- or many chlorophyte forms. Nevertheless, the ment by more diverse assemblages of species expectation is that epiphyte densities of 20 mg of richer lakes, before these too become elim- dry mass per cm2 would exceed their tolerance inated (De Nie, 1987). The complete transition, by macrophytes. Actually, such densities become to a turbid, phytoplankton-dominated system, is unstable and slough off periodically, although regressive on grounds of loss of diversity and the host plant would, by then, be unlikely to amenity, as well as a probable deterioration in derive much benefit. Depending on species com- the yield of fish. The mechanism of such tran- position, the chlorophyll a complement of the sitions was supposed to be light-mediated: as epiphytes might be 0.5–2.0% of the dry mass: the nutrients in solution increased, so did the phyto- critical epiphyte density of 10–20 mg dry mass plankton and, in consequence, light penetration per cm2 is equivalent to 0.05–0.4 mg chla cm−2, decreased. Even the intermediate replacement or 0.5–4 g chla m−2 of macrophyte leaf area. of low-growing charophytes by tall-stalked Pota- To compare this with the areal concentration mogeton (Moss, 1983) fits this explanation. How- of phytoplankton, or even of epilithic films on ever, it is only part of the story and it does the solid surface of rocks and stones, allowance not explain why species with floating leaves and must be made for the leaf-area index (the area theemergent reedswamp species should also fail of leaf surface per unit water area) (LAI). For a to survive. Work by Sand-Jensen (1977) had sug- LAI of ∼5, potential densities of epiphytes (on gested that the shading of epiphytes growing on this logic, up to 20 g chla m−2)wouldbefarin eelgrass (Zostera)significantly reduces light pen- excess of supportable phytoplankton or epiliths. etration to the leaf blade. At about the same Turning the calculation around, the theoretical time, Phillips et al.(1978)reportedfieldobserva- light-limited maximum active photoautotrophic tions and some supporting tank experiments in biomass that can be supported (∼120gCm−2) which the effect of epiphytic algal growth was to Fig. 3.8,Section 3.5.3) and the maximum phyto- smother the photosynthetic surfaces of the host plankton crops that are observed (range 30–50 g plant. Although a film of epiphytic algae is proba- Cm−2,say, 0.8–1 g chla m−2)would leave sub- bly a normal occurrence on the surfaces of water merged macrophytes already light-deficient. plants, Phillips et al.(1978) considered that the Of course, the epiphytic community of the increasing availability of nutrients in the water Aufwuchs is not exclusively algal and its chloro- column is as beneficial to epiphytes as to planktic phyll content is normally dynamic owing to algae. grazers. Macrophytes may be able to suppress ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 421 epiphytic and some planktic algae through the This hysteretic behaviour of forward and production of allelopathic substances (reviewed reverse switches has been successfully modelled in Scheffer, 1998), although, realistically, the by Scheffer (1990;see also 1998), using graphical principal influence over dominance is the compe- analysis. The model has stimulated further inves- tition for space, light and nutrients. This struggle tigative studies of the factors that most influ- is further influenced by the role of consumers – ence site-to-site differences in the trigger levels especially planktic filter-feeders and Aufwuchs of phosphorus and the response of the whole browsers. The complexity of these interactions system. make it difficult to predict their many potential outcomes. Nevertheless, some experiences of the Macrophytes and trophic relationships change from macrophyte to microplankton dom- The influence of fish on the operation of the inance of shallow lakes, and the reverse, focus on lower trophic levels is no less profound in the lit- the critical switches. toralworld of shallow lakes than it is in the The eventual loss of submerged macrophytes pelagic zone (Gliwicz, 2003b). In the absence as a consequence of progressive eutrophication of fish predation, filter-feeding crustacean zoo- of shallow lakes has often been found to be plankton can become sufficiently numerous to quite abrupt, presumably as a result of near- clear the water of algae. In macrophyte-rich simultaneous light inadequacy across a relatively ponds, however, alternations with algal abun- flat bottom. It is often the case that macro- dance are considerably damped, both in inten- phytes are either extensive across the lake, or sity and through time. The basis of this relative they are very nearly absent from a water col- stability seems to be that a low concentration of umn that is turbid with phytoplankton. Thus, large-bodied, filter-feeding cladocerans, involving these small, shallow lakes seem typically to exist genera such as Simocephalus, Sida, Diaphonosoma in one of two alternative steady states –either and the large Daphnia magna,isabletokeepthe they are macrophyte-dominated with clear water; water reasonably clear of phytoplankton. The sup- or they are phytoplankton-dominated, with fre- ply of locally generated and/or trapped organic quent high turbidity and a dearth of macro- debris, dislodged epiphytes and abundant detri- phytes (Blindow et al., 1993;Schefferet al., tus and bacteria from near the bottom provides 1993). an alternative and sufficient resource of filterable From syntheses based on the eutrophication organic carbon to support the stock of cladocera of a large number of shallow lakes in Europe, (Gulati et al., 1990). it appears that the change from macrophyte The presence of fish does not automatically to phytoplankton dominance occurs anywhere disrupt this stability. Cropping of zooplankton within a wide range of aquatic total phospho- by mature fish and 0+ (i.e. fry under 1 year rus concentrations (50–650 µgPL−1). These are in age) is not necessarily less intense in shal- arguably capable of sustaining phytoplankton low lakes than it is in deeper lakes. Indeed, and/or epiphytic algae of chlorophyll a at con- without the refuge provided by vertical migra- centrations likely to deprive submerged macro- tion, zooplankton is potentially subject to even phytes of adequate light. According to Jeppesen heavier predation. Several studies have revealed et al.(1990), many upward transitions occur in a that the behaviour of free-swimming cladocer- range 120–180 µgPL−1,inwhichthephosphate ans alters under the threat of fish predation, sequestering power of macrophytes is saturated exploiting the alternative refuge from ready vis- (Søndergaard and Moss, 1998). However, it does ibility offered by macrophyte beds. Horizontal not follow that a downward shift in phospho- migrations were first noted by Timms and Moss rusavailability will trigger a return to macro- (1984), the zooplankton moving into macrophytes phyte dominance in the same range. Indeed, it by day and moving into more open water in the seems that phosphorus concentrations need to hours of darkness. Moreover, subsequent stud- be rather lower than 120 µgPL−1 for the switch ies have demonstrated that the variety of species to work in the opposite direction (Moss, 1990). and the size classes of the cladocerans behaving 422 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

thus is directly related to the potential intensity duction (usually by large and persistent popu- of planktivory (Lauridsen and Buenk, 1996; Lau- lations of Planktothrix agardhii), robust, micro- ridsen et al., 1999). The experimental investiga- bially mediated recycling of autochthonous and tion of the behaviour of Daphnia magna (Laurid- allochthonous organic matter, and a food web sen and Lodge, 1996)showed a natural tendency comprising little but the larvae of Chironomus to avoidtheMyriophyllum plants was reversed in plumosus or C. anthracinus and benthic-foraging the presence ofsunfish (Lepomis cyanellus)andof carp, such as Cyprinus carpio. Most people find chemicals in the water in which the fish had this unattractive and believe its ecosystem health been recently present. In effect, the cladocerans to be poor but it is, nonetheless, a stable benefit from the presence of macrophyte beds state and also one that is ‘depressingly sustain- through reduced exposure to planktivory but able’ (Reynolds, 2000b). It is for these reasons remain sufficiently active to regulate the concen- that it is also very difficult to manage sites tration of phytoplankton and other forms of fine away from this kind of species structure with- particulate organic carbon. These are powerful out applying some fairly drastic environmental contributions to the short-term ecological stabil- engineering. ity of macrophyte-dominated systems. However, these are not continuous forces, nei- Biomanipulative management ther are they insensitive to changing fish den- The prospects for preventing and reversing the sities, species composition and feeding refuges, worst symptoms of eutrophication in small, shal- nor are they independent of macrophyte den- low lakes probably depend upon first recognising sity. High densities of facultative, opportunist thepresent state. Traditionally, the art of suc- and obligate planktivores in open water (in small, cessful biomanipulation is built upon the con- shallow lakes, this may refer mainly to young trol of phytoplankton abundance, which really percids and cyprinids, as well, of course, as means protecting the zooplankton. There are the 0+ recruits of most species) will eventually thus threshold levels of planktivory that should overcome the capacity of cladocerans to clear not be exceeded. Even then, phosphorus availabil- thewater. Encouraging piscivorous predation on ity may still bias against macrophytes, whose col- planktivores (for instance, by stocking, with pike, lapse will precipitate the loss of a viable agent in Esox lucius)should assist in keeping their impact maintaining water quality. on the zooplankon within its critical threshold Quite clearly, if habitat quality once slips to intensity and, thus, in upholding and enhancing that level, then recovery demands that the tight the stable, macrophyte-dominated state (Grimm linking among the minimal components of the and Backx, 1990;Beanand Winfield, 1995). Other- whole system is broken. This may require drastic wise, phytoplankton may be released from effec- reductions by netting of stocks of cyprinid fish tive control and the balance in favour of macro- (roach, Rutilus;bleak, Alburnus;bream, Abramis; phytes, supposing that they really do dominate carp, Cyprinus carpio), as well as small individu- the material transfers within the existing sys- als of non-cyprinid species. It may also require tem, may quickly be turned against them. More- thedredging out of the unoxidised sediments over, with the foraging of the facultative plank- and/or routine flushing with less nutrient-rich tivores focused on benthic invertebrates (see Sec- water. The assisted re-establishment of appropri- tion 8.2.2), there isanincreasingriskthatthe ate macrophytes and their protection from graz- weakened macrophytes are uprooted and dis- ing birds (such as coot, Fulica atra)mayprepare lodged. Sediments are increasingly liable to tur- theway forrestocking with non-cyprinid fish. bation with further feedbacks towards macro- Such restorations are cumbersome and expen- phyte exclusion by turbidity and loss of refuge sive to apply and the precedents have achieved for zooplankton. The whole system can quickly only varying degrees of success. Needless to say, experience a rapid ‘regime shift’ (Carpenter, instances of successful, self-sustaining biomanip- 2001), towards a simplified, low-diversity struc- ulative management have been attained before ture based upon copious planktic primary pro- theundesirable phytoplankton-dominated steady ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 423 state has become too firmly established (Hos- ies, the concentrations of acidic gases and radi- per and Meijer, 1993). Often, it is sufficient cals and the concentrations of neutralising bases to intervene before the ‘forward switches’ have determine the hydrogen ion concentration in operated. Over-management of macrophytes and lakes and seas. Lakes are, or become, acidic when overstocking with fingerling fish, both perpetra- theinput of hydrogen ions exceeds the amounts tions of single-minded but misinformed anglers, of neutralising bases gleaned from the water- have predictably deleterious impacts on zoo- shed through the weathering of rocks. Phyto- plankton stocks and the objective of limpid water. plankton production in the lake also helps to Once the stability of the macrophyte- reduce acidity through the uptake of nitrate, sul- dominated state has been threatened, greater phate and carbon dioxide gas dissolved in the control over planktivore stocks must be exer- water. cised. Based on the investigations of Gliwicz The simple methodology for estimating the and Preis (1977)onthe direct impacts of plank- hydrogen-ion concentration (expressed as a nega- tivory on zooplankton, it would seem unwise tive logarithm, the pH) allows us to record it with to allow the fresh biomass to exceed 300 kg some diffidence. The effects of photosynthetic ha−1 (30 g m−2,about6gCm−2); to do so withdrawal of carbon dioxide and the buffer- would impair the sustainability of secondary pro- ing provided by the dissociation of the weakly duction yields (see Sections 6.4.2, 8.2.3). Stock- acidic bicarbonate ion have been discussed ear- ing of benthic foragers (carp, bream and tench, lier (see, especially, Sections 3.4.2, 3.4.3). The car- Tinca tinca)should be avoided. It may be nec- bon dioxide dissolved in precipitation (rainfall, essary to exclude bottom-feeding ducks, coots snow, condensation) comes from the atmosphere. and other rails. Other ‘reverse switches’, includ- The natural pH of rainwater may be between 5.0 ing the reduction of nutrient loading, should be and 5.8, depending upon contemporary temper- applied if feasible. For fuller advice and guidance ature and pressure conditions and the extent of on applying biomanipulative techniques, any of carbon dioxide saturation. The particular prob- theexcellent manuals now available should be lem of ‘acid rain’ begins with the anthropogenic consulted (Hosper et al., 1992; Moss et al., 1996). enhancement of the products of oxidation – oxides of carbon, sulphur and nitrogen – in the 8.3.7 Phytoplankton and acidification atmosphere. There, solution and reaction with Acidic waters are not unnatural but anthro- liquid water results in the enhanced formation pogenic acidification of rainfall and land of strong acids (H2SO3,H2SO4,HNO3). On contact drainages has impacted upon aquatic ecosystems with the ground, acidic precipitation may be neu- with effects quite as deleterious as those imposed tralised or rendered more or less alkaline by the + + by nutrient enrichment. However, the behaviour bases (carbonates of Ca and Mg, K ,Na and NH3) of phytoplankton is rather less central to the that it dissolves. Alternatively, rainwater pass- perceived environmental damage through acid- ing across impervious catchments dominated by ification than it is in the case of eutrophication. granitic, dioritic and other weathering-resistant The restoration of acidified water bodies is not a rocks acquires little base or alkaline buffering major concern of the present section; rather, the capacity. Accordingly, lakes and rivers draining relationships between phytoplankton and envi- catchments in which the buffering capacity is ronmental excesses in the hydrogen ion concen- generally poor, achieving alkalinities of ≤0.2 meq tration are the main focus. L−1,areparticularly sensitive to ‘acid rain’. Natural water supplies to lakes and seas At first, the symptoms of acidity generation are not pure. Characteristically and distinctively, were recognised mainly in the immediate down- they contain varying amounts of numerous wind localities of industrial and domestic fuel- solutes, leached from the atmosphere and from burning: areas of northern England and western the terrestrial catchments with which the water Germany were once very badly affected with dam- has been in contact. In much the same way age to trees and buildings, loss of soil fertility as nutrients are loaded on receiving water bod- and lowered pH of drainage water. Through much 424 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

of the industrial period, these effects were sec- aquatic ecosystems have come from base-poor, ondary to (but they compounded) the more obvi- high-rainfall upland areas, where the inherent ous consequences of the deposition of unburned neutralising capacity is least: northern Europe carbon (soot). Analogous problems arose from (Scotland, Fennoscandia and, especially, the Tele- ore-smelting in the area of Sudbury, Ontario. As mark area of Norway) and certain Shield areas of much to deal with local air-pollution problems Canada. as for any other reason, a progressive switch was The impacts of acidity on aquatic ecosystems made to alternative, more completely burning invoke several mechanisms. Besides having to fuels that are combusted at higher temperatures, cope with an excess of hydrogen ions, low pH whilst waste gases were vented higher into the affects the chemistry of several elements of bio- atmosphere. At the same time, the total con- logical importance. One obvious consequence of sumption of carbon-based fuels fuel has greatly thedirect sensitivity of calcium carbonate sol- expanded, with the result that local problems ubility to pH affects the tolerances of shell- of poor air quality and noxious deposition were building molluscs and carapace formation in the replaced by a global one of acidified precipita- crustaceans (Økland and Økland, 1986). Also crit- tion. It is not, however, a straightforward case ical is the solubility and aluminium ions which of a universal and systematic lowering of the are extremely toxic to organisms not equipped to pH of rain: depending upon the provenance of deal with them (Brown and Sadler, 1989;Herr- aparticular airstream and its recent history of mann et al., 1993). Metals, including iron and rainfall elution, precipitation is much more sub- manganese, may be activated to harmful levels ject to what are sometimes termed ‘acid events’ through the disruption of dissolved humic com- (Brodin, 1995). Since the mid-1980s, some ame- plexes (DHM) (see Section 3.5.4). lioration has come through better understand- Aquatic organisms vary in their sensitivity ing and recent international concord has secured to low pH and elevated concentrations of alu- cuts in the emissions of strong acids to the atmo- minium and manganese. Examples of species sphere. The expedient of burning natural gas in (or races) of fish and invertebrate that are tol- preference to oil or coal also generates less sul- erant of high acidity levels have been docu- phate per unit energy yield. Nevertheless, there mented (by e.g. Almer et al., 1978). However, can be few locations on the Earth where rain- those close to the extremes of physiological tol- fall does not, at times, continue to deposit abnor- erance may suffer catastrophic mortalities as mally enhanced loads of acid. a consequence of a relatively small downward In the present context, the concern lies in the drift in pH during a single acid event. Among precipitation after it has reached the ground. It themacroinvertebrates, only insects seem tol- is early on in its percolation into a well-formed erant of high acidity (Henrikson and Oscar- soil and its throughflow to the surface drainage son, 1981). Investigations of known acid-tolerant that the chemical composition of the drainage to species of phytoplankton have revealed a bio- rivers and lakes is mainly determined. It is quite chemical mechanism in Chlorella pyrenoidosa, apparent that the natural acidity of rain is nor- Scenedesmus quadricauda (Chlorophyta) and Euglena mally quickly neutralised by the bases present mutabilis (Euglenophyta) for regulating internal and which, generally, are derived from the weath- pH against high external H+ concentrations (Lane ering of parent bedrocks. However, where rocks and Burris, 1981). However, the ability of E. muta- are hard or slopes are steep, soil cover is thin bilis to deal with mobilised aluminium species and bases are deficient, the acidity is not over- (Nakatsu and Hutchinson, 1988)maybethe come and it registers in the lake water. Acidity decisive specialist defence against extreme acid in drainage may actually be enhanced by cer- enviromnents. tain types of vegetation exchanging hydrogen Some algae, including desmids (Cosmarium, ions for valuable nutrients. Thus, as already indi- Cylindrocystis)andeustigmatophytes (Chlorobotrys), cated, almost all the reported instances of pro- are characteristically associated with acidic pools gressive acidification rising to levels damaging in wet Sphagnum bog. Among the freshwater ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 425 phytoplankton, tolerance of natural high acid- carbonate/bicarbonate reserve. Another interest- ity is shared among a number of other species ing and controversial alternative approach that (see, for instance, Swale, 1968;Nixdorf et al., has been devised recently involves the deliber- 2001), many of which do happen to be flag- ate addition of phosphorus to the water (Davison, ellated chlorophytes or euglenophytes. Species 1987). It was successfully applied to secure the of Chlamydomonas, Sphaerella, Euglena and Lep- restoration of a series of highly acidified former ocinclis are frequently encountered in small sand workings in eastern England (Davison et al., acid lakes, one or other usually dominating 1989)and, later, to the restoration of an acidified alow-diversity population. Cryptophytes (Pla- upland tarn in the English Lake District (Davison gioselmis, Cyathomonas), chrysophytes (Ochromonas, et al., 1995). Davison’s (1987)original stoichiomet- Chromulina)and dinoflagellates (Gymnodinium, ric calculations led him to propose that phospho- Peridinium umbonatum)arealsorecorded, as are rusis47times more effective in generating base certain non-motile chlorococcalean species of than the molecular equivalent of calcium carbon- Chlorella and Ankistrodesmus. Some species of the ate. In extreme cases, lime may still be needed to diatom genera Eunotia and Nitzschia are also bring the system to a pH level at which phos- known to be acid tolerant but most planktic phorus addition will promote the development species of Cyanobacteria do not grow at pH levels of a biotic community and the consumption of much below 6.0 (H+ ≥ 1 µmol L−1). acidic anions. In each of the restorations thus Swale (1968)recorded occasional large pop- attempted, a single or pulsed addition of phos- ulations of Lagerheimia genevensis and a 14- phate was sufficient to maintain an alternative month period of dominance by Botryococcus brau- planktic community, often with new species of nii in Oak Mere, England (contemporaneous pH algae and crustaceans, submerged macrophytes 4.7–4.9). In the extremely acid lakes left by lig- and fish, for long periods of time measurable in nite mining in Lusatia, Germany (pH 2.3–2.9), units of hydraulic residence time. Lessmann et al.(2000)notedthepresence of This may not be a universally acceptable Scourfieldia and a Nannochloris,andtheeugleniod approach to managing lakes, especially among E. mutabilis.Inthe highly acidic caldera Lago managers who have craved the virtues of phos- Caviahue, Patagonia, Argentina (pH 2.5, i.e. acid- phorus reduction as a route to high water quality ≥4mmolH+ L−1), the phytoplankton was ity (Reynolds, 1992a). Their perplexity is easy found by Pedrozo et al.(2001)tobedominated to understand; phosphorus addition could eas- by a single green alga, Keratococcus raphidioides. ily contribute to a worse problem than the one Indeed, this alga, a subdominant Chlamydomonas to be overcome. On the other hand, overzealous and a single bdelloid rotifer comprised the full pursuit of phosphorus limitation strategies has list of recorded planktic species. Species selec- sometimes reduced the ability of base-poor lakes tion in the lake may also be influenced by the to resist the effects of strong-acid precipitation low nitrogen content of the water and its rela- and the loss of their fish populations. Careful tively high concentrations of the metals Fe, Cr, Ni analysis of the respective loads and fates of hydro- and Zn. genand orthophosphate ions could lead to more The application of restorative treatments to imaginative strategies for management offer- lakes that have become artificially acidified is ing longer-lasting benefits to biological water generally considered if it benefits commercially quality. important fish species or viable fisheries. The usual method is to apply lime to the water 8.3.8 Anthropogenic effects on the sea or to relevant parts of the catchment (Henrik- Nutrient enrichment of the oceans, at least as son and Brodin, 1995;Hindar et al., 1998), Lakes aby-product of human activities, has not been can be assisted to move back towards neutral- widely considered as an issue on the scale that ity and to acquire a fully functional, healthy, it has become among inland waters. This does pelagic ecosystem. Acidity is consumed and pro- not mean that anthropogenic eutrophication of gressively more of the carbon dioxide enters the the sea is necessarily a lesser problem, nor that 426 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

we should not question a popular notion of rais- Away from the shelves and distant from tering the fertility of the ocean in order to enhance restrial influences, the nutrient content of the its role as a sink for atmospheric carbon diox- upper oceans is plainly subject to depletion ide. However, both are probably overshadowed through uptake by autotrophs but the variations by problems arising from gross anthropogenic remain within levels representing approximate distortion of the structure and geometry of the contemporary maxima (∼2 µMP,20–40 µMN marine food webs. Let us examine these issues in and ∼160 µMSi(seeSections4.3.1, 4.4.1 and 4.7). sequence. Actual concentrations in surface waters are generally rather lower than these levels, with, typically, the residual concentrations suggesting that Eutrophication of the seas available nitrogen is more vulnerable to exhaus- Given the vastness of the oceans, compared both tion by autotrophic growth than phosphorus. to the tinytotal area of inland standing waters However, as acknowledged and verified by exper- and to the scale of human impacts on global imentation, the capacity-regulating element in nutrient cycles, it is probably not at all surprising the upper ocean is iron, where maximum lev- that oceanic systems remain resolutely ultraolig- els may be one or two orders of magnitude less otrophic and support such low levels of biomass. concentrated than 10−3 µM (Martin et al., 1994; On the other hand, the modest levels of biomass Section 4.5.2). and production that they do support are not Thus, the open oceans remain steadfastly olig- controlled primarily by the fluxes of nitrogen otrophic in potential and in their performance. and phosphorus but, more probably, by the sup- On the principle that, at low levels of limiting ply of bioavailable iron or of inorganic carbon nutrient availability, any increase in supply will and, for long periods in most latitudes, by the raise the carrying capacity by a corresponding hydrodynamics of vertical mixing and the depri- margin, then the pelagic biomass is most sen- vation of light. It is in the relative shallows of sitive to a change in iron availability. Without the continental shelves and at the coastal inter- this, indeed, enrichment with other nutrients faces with the land masses, where the iron, car- will not stimulate classic eutrophication effects. bon and light-dilution constraints are simulta- One corollary is that autotrophic production and neously assuaged, that the enriching effects of the biomass-carrying capacity of the ocean (and terrestrial sources of nitrogen and phosphorus thus its role as a carbon sink) can be stimulated are already well known. For instance, in their by seeding the ocean with bioavailable iron (see review of transport processes and fates of ter- pp. 428--31 below). restrial phosphorus, Howarth et al.(1995)estimated that current inputs to the sea have tre- Anthropogenic impacts upon marine bled since the pre-agricultural period. There are communities and food webs likely to have been significant increases in inputs At present, the greater anthropogenic impacts to of inorganic nitrogen (chiefly as nitrate) during the health and functionality of marine ecosys- the twentieth century but, as concentrations in tems come from a series of devastating assault shelf waters and oceanic surface waters typically on the structure of marine ecosystems. These continue tobedepletedto<2 µmol N L−1 (<30 include destructive alterations to coastal habi- µgNL−1), increasing biomass capacity remains tats, pollution and increasingly industrialised in the control of nitrogen availability. Interest- methods of protein harvesting from the sea. ingly, recent increases in planktic biomass in the Mostly, they are relatively local in concept and Baltic Sea have been among the nitrogen-fixing in execution but, cumulatively, their impacts are Cyanobacteria (notably Anabaena lemmermannii, alarming. In a thoughtful review, Jackson and Aphanizomenon flos-aquae and Nodularia spumige- Sala (2001)summarised the effects of widespread nea)inresponse to progressive increases in phos- coastal engineering, pollution, turbidity and fish- phorus loads from adjacent land masses (Kuosa ing activities in damaging coral-reef habitats, the et al., 1997). truncation of temperate kelp forests and their ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 427 replacement by ‘sea urchin barrens’ of crustose thus, the lack of an economic incentive to bet- algae. In Europe, competing demands for the termanage it in a way that does not lead to its exploitation of the land surface in valley flood overexploitation. The third is that the industrial plains are driving the winning of sands, grav- momentum is in advance of the ecological knowl- els and other building aggregates into increas- edge to set sustainable levels of exploitation ing intensities of offshore coastal dredging. It is on the underpinning relationships of biomass, inevitable that the process removes entire ben- production and energy flow through pelagic thic food webs and generates clouds of turbid- ecosystems. ity in its wake. These may be short-lived impacts It is not even clear that, were such knowl- while there are adjacent ‘islands’ whence biota edge available, informed guidance would be fol- can re-establish but it is not clear how well cur- lowed. Long traditions in the study of growth rent practices allow this. and recruitment in fish populations (Beverton At another level, Jackson and Sala (2001) cat- and Holt, 1957; Ricker, 1958;Cushing, 1971, 1988: alogued the diminution in large animals that Cushing and Horwood, 1977) and their match or were once ‘keystone species’, linking structure otherwise to environmental conditions (Cushing, to energy flow (see Section 8.2.4)and maintain- 1982, 1990, 1995)havenotbeen abletoavert ing the pristine coastal ecosystems of which well-documented stock-recruitment collapses of they were once part. Loss of these animals the herring (Clupea harengus)intheNorth Sea or has contributed to significant habitat changes. of the northern cod in the north-west Atlantic, Declines in grazing and foraging by manatees around the Labrador Grand Banks (see Cushing, (Trichechus spp.) and dugongs (Dugong dugon)have 1996). The contested imposition of quotas now allowed former sea-grass meadows to develop looks like actions that were ‘too little, too late’ into dense stands. The top layer of predators in as the symptoms of collapse show very early. coral reefs (tiger sharks (Galeocerdo cuvievi), monk The ultimate truth of the maxim that ‘fisheries seals (Monachus spp.)) has been reduced with cas- that are unlimited become unprofitable’ (Gra- cading effects on coral consumers. Destruction of ham, 1943)isupheld. cod (Gadus morhua)stocksandsea otters (Enhydra In recent decades, the issues have only intensi- lutris) has released from control the sea urchins fied. Fishing fleets now scour continental shelves. that now interfere with kelp regrowth. Trawlnets are built to be dragged along the sea Some of these changes are the direct effects of floor where they sweep up all in their path for the human overexploitation of the animals in ques- prize of a few more demersal fish. The imposition tion, either for food or fur. Others are the indirect quotas for size and species catches can only be consequences of the diminution of the exploita- controlled after sorting, when most of the ‘illegal tion, either through the vacation of a foraging excess’ is returned to the water dead. Indeed the niche to competitors, or to the relaxation of crop- catching methods are still so coarse that fishing ping of lower trophic levels. It is perhaps 4000 can scarcely be directed to catch preferentially years (4 ka) ago that Homo sapiens entered the therelatively plentiful fish. Conventional ecolog- marine food web by catching predatory fish and ical theory suggests that, where interventions are mammals in their natural environments (Cush- targetted successfully at a particular dominant ing, 1996). However, it is mainly within the last species, then another with similar environmen- century and, especially, the last 30 years that tal requirements and dietary preferences and the industrial scales of sea fishing, backed by such next highest exergy potential (i.e. the next best technological sophistications as sonar and satel- competitor) should be poised to assume that role lite tracking that the hunter–gatherer approach (Wardle et al., 1999; Elliott et al., 2001b)(expla- to foraging has descended to plunder and loot- nation in Section 7.3.4). This is roughly what ing. The trouble is threefold. One is the economic happened in the North Sea: following the severe drive for a return (through the sale of catches) reduction in herring, there was an ‘outburst’ of on the investment in ships and crews. The sec- several gadoid species, including cod and had- ond is the lack of ownership of the resource and, dock (Megalogrammus aeglifinus). The reasons are 428 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

complicated, however, and include the possibility rent trends in global warming has been referred of reduced herring predation on cod larvae and to in Section 3.5.2.Burning coal, gas and oil the greater availability of Calanus larvae to young is generating a flux of carbon dioxide from cod, now relatively freed from consumption by the Earth to the atmosphere equivalent to 7.1 herring. One of the problems of the largely uns- (±0.5) Pg a−1. Despite the Kyoto Accord, this elective trawling of those same cod stocks is that is likely to go on increasing until demand it is unlikely to leave many demersal contenders or depletion of the relatively readily accessi- to fulfil its role. Thus, a further trophic linkage ble parts of the global reserve (estimated to be is compromised. ∼5000 Pg) raise the cost sufficiently to make Following similar logic, the industrial fish- it competitive to exploit other energy sources. ing of species with other commercial value (for Apart from its contribution to acidity, carbon instance, for the purpose of manufacturing fish- dioxide is one of the atmospheric gases (with meal and the extraction of fish oils and pro- watervapour and ozone) that absorb much of teins) may be depleting shelf waters of their diver- the long-wave terrestrial radiation back-reflected sity and of the ability to support other mar- from the Earth (chiefly in the wavebands 2–8 and itime species (birds, seals, whales). Of yet fur- >14 µm). Thus, its accumulation in the atmo- ther concern should be the ‘creaming off’ of the sphere might enhance the so-called ‘greenhouse higher levels of the oceanic food chain of the olig- effect’ and contribute to global warming. The otrophic oceans; catches of such species as tuna extent of effects directly attributable to the accel- (Thunnus), barracuda (Sphyraena), sea-bass (Morone) erated oxidation of organic carbon is still not and others are commercially very attractive but clear. On the other hand, such a scale of inter- probably unsustainable at present rates. vention into the natural planetary cycling of car- The science and the economics of overex- bon is unlikely to avoid significant consequences ploitation of fisheries are not the principal con- on average planetary temperatures, climatic pat- cern of this book, though it does recognise that terns and sea levels. urgent action is required if the excellent source Many insist that the changes have already of healthy protein and oils is to remain available. commenced and there is a growing, general (but It is clear that farming of commercially impor- not universal) political consensus that ‘some- tant fish species (as opposed hunting and gather- thing must be done’. Simply cutting back on the ing them) is no more sustainable while it requires consumption of fossil fuels would be an obvious the continued fishing of other species to provide step but cheap and available energy is a drug, feed. Nothing less than the total exclusion of all addiction to which is economically too painful fishing fleets from large stock-recruiting areas is to abandon. There are problems of political equi- going to assist the survival of viable and function- tability over the consequences of therapies and ally intact food webs. The consequence of doing over the cost-sharing of the alternative energy nothing is likely to be a fairly rapid slide towards sources. apelagic ecosystem that effectively comprises lit- Another idea, seriously advanced as a means tle more than phytoplankton, mesozooplankton of stabilising atmospheric carbon dioxide lev- and macroplankton. els, is that we could augment the flux of carbon dioxide from atmosphere to ocean. The suggested mechanism is to raise the fertility of the Anthropogenic countermeasures to the sea, so that more carbon might be fixed in pho- atmospheric accumulation of greenhouse tosynthesis into more biomass, and with more gases being consigned as export to the deep ocean. By The irrefutable evidence for the increase in implication, the key players invoked are members atmospheric carbon dioxide during the indus- of the marine phytoplankton, so the idea must trial period (caused by the oxidation of fos- command the attention of readers of this book, sil fuels and of humic matter in agricultur- requiring a careful consideration of its logic and ally improved land) and its likely role in cur- thelikely consequences of its implementation. ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 429

Starting with what we know, the global stores supposed to increase the capacity for its storage and fluxes between atmosphere and ocean are in the sea?’ already impressive. Using the tabulated data of One part of the answer is another question – Margalef (1997), the atmospheric store (presently ‘Ifsolittle does so much, then how much more around about 650 Pg C) is currently increasing by could a little more do?’ Put another way, ‘Will about 3.3 Pg a−1. Thus, the net burden of anthro- abigger primary producer biomass not increase pogenic carbon emissions to the atmosphere is the flux of carbon dioxide to the ocean, per- currently countered by an annual removal of car- haps to the point of balancing the anthropogenic bon dioxide of some 3.8 (±0.5) Pg C a−1. These excesses?’ How, indeed, can we be sure that are not trivial amounts but, on the scale of the adding nutrients does not simply accelerate the natural biogenic fluxes, they are comparable with cycle, with the wheel spinning faster rather than theerror terms of primary production (Table 3.3). increasing in mass? This must be a serious pos- Terrestrial net primary production (56 Pg C a−1) sibility if we follow the deduction that the net maintains a biomass (including wood) of about yield of exportable primary product across most 800 Pg C and a store of other organic necromass of the open ocean is tolerably close to the likely of about twice that (1600 Pg C). These are not invasion rate of carbon dioxide across the sur- static amounts but present rates of forest clear- face of the sea (Sections 3.4.1, 8.2.2). A rising ance and land drainage probably impede any cur- flux of carbon dioxide, driven by an increasing rent net increment to the storage capacity. By partial pressure in the atmosphere, might raise deduction, much of the missing 3.8 Pg C a−1 is the sedimentary flux by the same few percent- already dissolving in the sea, assisted by increas- age points but, mainly dependent upon microbial ing partial pressure. In any case, the quantity processing, enhanced exports depend as much of carbon dioxide in solution in the sea (some upon faster turnover through the web. Then, rais- 40 000 Pg) makes it by far the largest store of car- ing the fertility of the medium might lift the bon in the biosphere. This does not mean that the supportable biomass at successive trophic levels, additional input to the dissolved carbon dioxide including the larger consumer categories that pool is necessarily insignificant. We should bear are likely to provide the desired increases in car- in mind that the additional gaseous load is to bon exports. Moreover, the deep oceans are capa- the immediate surface layer, where its involve- ble of storing a lot more carbon dioxide in solu- ment in the carbon dioxide–bicarbonate system tion without the net ‘outgassing’ evident among (see Section 3.4.1 and Fig. 3.17) and a net depres- small lakes (see Section 8.2.3). What is required sive impact upon pH will make it increasingly is the minimisation of C cycling in the micro- difficult for carbonate-deposting phytoplankters bial loop of the surface waters and the numerous (such as coccolithophorids) and animals to form opportunities it offers for the venting of carbon their calcareous shells. dioxide as a primary metabolite and, instead, to The desired fate of the additional carbon diox- direct fixed carbon into exportable, sedimentary ide flux is that it should be taken up by enhanced biomass phytoplankton photosynthesis. Currently, net pri- This is easily stated but it is a formidable hur- mary production in the sea (48 Pg C a−1), impres- dle to overcome. Let us recall the viscous envi- sively generated by a producer mass equivalent to ronment of oceanic primary producers (Section ≤0.7 Pg C, supports an average oceanic biomass of 2.2.1), in which viscosity is a more significant ∼10 Pg C and which is, self-evidently from these force than gravity, and vertical transport is rel- figures, turned over very rapidly. A large propor- evant primarily in the context of exposure to tion of the organic carbon fixed in phytoplankton underwater irradiance (Section 3.3.3). The supply photosynthesis is respired back to carbon dioxide of nutrients (some albeit very scarce) is medi- without leaving the euphotic zone. Our first ques- ated primarily by molecular diffusion (Section tion might be: ‘How is such a small part of the 4.2.1). Though species composition may vary, the global biomass, itself already involved in 40% of structure of the food web and the relative pro- the short-term movements of biospheric carbon, portionality of mass among its components (the 430 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

producers, heterotrophs and microphagotrophs) solution of the siliceous walls) before they have are, within certain limits, highly conserved (a settled more than a few tens to hundreds of point elegantly emphasised by Smetacek, 2002). metres through the ocean (Reynolds, 1986a). Of The effect of pulsed enrichment by an other- course, the aggregation of dying cells into larger wise limiting resource should benefit the growth flocs (up to and including ‘marine snow’ (All- ratesofall microbes alike. However, photoau- dredge and Silver, 1988;see also Section 2.5.4) totrophs are uniquely able to invest resource may accelerate the rates of sinking and slow the in new biomass whilst simultaneously cutting ratesofdecay (Smayda, 1970). In this way, the net the overspill of carbon to the heterotrophs. export of diatom and other POC in the form of At thesame time, bacterial populations suffer ‘phytodetritus’ is enhanced (Legendre and Rivki, the ongoing constraints of protist grazing and 2002a). viral pathogens. Thus, for a variety of reasons, While oceanic production is concentrated in thestructure of the fertilised microbial web the picoplanktic prokaryotes and is intimately is distorted in favour of pico- and nanoplank- coupled to the microbial web, it is easy to under- tic producers and disproportionately against the stand why diatom-based export of unoxidised smooth flow of carbon through to an exportable POC beyond the upper ocean is abnormal and flux of mesoplanktic consumers or food to fish. event-led(Karl,2002;Karlet al., 2002). In this con- More and more sustainable phytoplankton is not text, the phytoplankton biomass of the coastal at all an ideal carbon sink while it largely stim- and shelf waters, which is responsible for about ulates only producer biomass. Above unspeci- aquarter of the net primary production of the fied thresholds (though probably in the range sea (Table 3.3), is more continuously and more 0.01–0.1 mg C L−1), the concentration of phy- conspicuously populated by diatoms, dinoflagel- toplankton carbon (together with other detrital lates and coccolithophorids. Globally, coastal and sources of POC) may permit the short-circuiting shelf systems are already likely to be playing a of the microbial loop and the imposition of direct significant part in the export of biogenic carbon mesoplanktic herbivory on algae. Above 0.1 mg C out of the surface circulation (Bienfang, 1992). L−1,thisisstillmorelikely to be true, asthe Moreover, parts of these same shelves are already threshold concentrations of many types of plank- sites for the accumulation of inwashed terres- tic filter-feeder are saturated (Section 6.4.2). trial detritus and POC, and where the concern Thus, the critical cue (singularity: Legendre over nutrient limitation of carrying capacity has and LeFevre, 1989;seealsoLegendre and Ras- been more to prevent its increase rather than to soulzadegan, 1996)toenhanced carbon export encourage it. from surface waters is to promote sustainable To recap, the uncertainties about the likely pelagic structures producing either readily graze- effects of oceanic fertilisation on the atmospheric able levels of nanoplankton (and the attendant carbon dioxide content are too many and too flux of faecal pellets) or predominantly sedimen- great to advocate its deployment as a strategy. tary microplankton. In the contemporary ocean, The impressive results of the IRONEX and SOIREE large-celled diatoms are usually the main agents fertilisations of the iron-deficient Pacific (Martin of the sedimentary export flux of organic car- et al., 1994;Bowieet al., 2001;seealso Section bon (Falkowski, 2002), especially at times of accel- 4.5.2)might offer a persuasive case for emula- erated production, beyond the control of the tion on the basin scale. However, supplementing microbial food web (Legendre and Rassoulzade- theiron supply in a low-latitude ocean would gan, 1996). only raise the ceiling on producer mass to the This behaviour is generally attributable to the scale of the next capacity limitation (nitrogen) relatively high sinking rates of diatoms (Smayda, and not at all where iron is not already limit- 1970;seealsoSection 2.5). However, the fastest ing growth. Under these circumstances, the most sinking rates of settling individual cells are prob- likely consequence of iron enrichment would ably inadequate to prevent the death and decom- be, presumably, the promotion of nitrogen-fixing position of the protoplast (and even the re- prokaryotes, with little benefit either to the ANTHROPOGENIC CHANGE IN PELAGIC ENVIRONMENTS 431 carbon-exporting elements of the pelagic food come. Even the extrapolations on which the cur- webortothe growth of diatoms. According to rent fears about climate change are based may Legendre and Rivkin (2002b), the frequency, quan- be quite wrong, with the response of global tem- tity and composition of nutrient additions would peratures to the rise in greenhouse gases being greatly bias the structure of the planktic com- either overestimated or frighteningly underesti- munity. Frequent additions of nutrients offering mated in its effects on human civilisations. The high ratios of Si to both N and to P are necessary latter might yet persuade us to adopt appropriate to promote diatom dominance. For the produc- countermeasures. However, doing nothing but tion of blooms to sink to depth ungrazed, any allow the planet to adjust its carbon fluxes and matching of nutrient additions to grazer demand stores might be a prudent option, even though it must be avoided. It is clear that there is no simple probably carries enormous social and economic strategy for enriching tropical seas that does not discomforts to humankind. risk chaotic or undesirable consequences. Out- The contemporary view of the role of the side the tropics, the most likely capacity con- oceanic biota in the global carbon cycles has straint upon phytoplankton is an insufficiency of been elegantly encapsulated in Falkowski’s (2002) light, which no amount of fertilisation will over- overview. The diatoms are the major exporters come. Shallow coastal waters offer the only real of organic carbon (with silica) to the sediments; prospect for accepting more carbon into biomass the coccolithophorids are major exporters of carbon and then transporting ittodepth.Itis calcite (calcium carbonate). This arrangement not clear that such waters are strongly nutrient has persisted for over 100 Ma, really since tec- deficient. However, the grave distortions to the tonic upheavals and continental drift effectively food webs of the continental shelves, mentioned opened up new niches for exploitation (see also in the previous section,make the impacts of fur- Section 1.3). Throughout that period, there has ther fertilisation on the structure and function been a progressive reduction in the atmospheric of their surviving components still more difficult carbon dioxide content (from about 700 to 280 to predict. p.p.m.). This may be due largely to the rate of Abettercandidate for taking forward the subduction of carbonate-rich oceanic sediments principle of enhanced carbon dioxide sequestra- exceeding the rate of volcanic and orogenic car- tion by marine primary producers is surely fur- bon dioxide generation, throughout the Cenozoic nished by kelps and other large seaweeds. These period. The planet has cooled sufficiently for the at least have the merit of accumulating (rather ice caps to form, for the sea level to fall, exposing than simply metabolising) the carbon they absorb areas of continental shelf, and for the planet to and, moreover, in a form that is conveniently become drier. harvestable, compostable and combustible as bio- Following the establishment of polar ice, fuel. Seaweed growth is naturally even more con- the Milankovitch cycle of climatic oscillations, fined to unpolluted shallow shelf waters than is caused by rhythmic orbital variations of the phytoplankton. However, if the provision of suit- Earth around the Sun (with a frequency of 90–120 able artificial substrata could be devised, such as ka) and resultant variation in solar radiative floating mats on which the seaweeds could estab- forcing, has been marked by significant glacia- lish, then the potential of the marine system to tions. The last four, at least, saw the expan- remove of more carbon dioxide from the atmo- sion of the Arctic ice cover over large parts of sphere might begin to be achievable. thenorthern hemisphere. The interactive role of the biotic oceanic carbon cycle with climatic Phytoplankton and the future variations through the last 400–500 ka are now The balance of wisdom should be against delib- well understood, through the combination of erate manipulation of the marine phytoplank- radiocarbon dating and stable-isotope analysis of ton tomopup anthropogenic carbon dioxide. biogenic deposits with atmospheric fingerprints Present knowledge provides an inadequate basis of contemporaneous layers in ice cores. With forreliable and precise anticipation of the out- theonset of a glacial period, terrestrial plant 432 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

production decreases and significant amounts overtake the scale of Cenozoic fluctuations and of carbon are transferred from the land to the match the temperature rises of the late Permian, sea. The process is reversed during interglacials. which brought life on earth close to extinction Sea levels fall as ice volume increases, exposing (Section 1.3). coastal lowlands to oxidation and erosion and the Neither prospect – being baked or suffering release of nitrogen and other nutritive elements violent climate change, lowland inundation and to marine ecosystems. Increased nutrient delivery massive economic disruption – is at all comfort- to inshore waters stimulates production of large- ing to humankind. However, the prospects for the celled phytoplankton and the export of more car- microbial engineers of atmospheric and oceanic bon to depth. Drier climates also allow more composition, including the phytoplankton, are wind-blown dust and the aeolian fluxes of min- mostly good. Their ability to go on regulating the erals, including iron, to the sea are raised. These planet, while other species have come through changes in the nutrient availability drive accel- and caused desolation, seems to be assured. erated carbon dioxide exchanges, with increased leakage back to the atmosphere. Falkowski (2002) analogised these exchanges to the ocean ‘breath- 8.4 Summary ing’ in and out on a 100-ka cycle, inhaling carbon dioxide from terrestrial systems during glacial The chapter seeks to evaluate the importance periods and exhaling it during the interglacials. of phytoplankton to pelagic function and to Because these exchanges feed back positively on thebiogeochemical role of pelagic domains to the Milankovich-driven variations, it is reason- thebehaviour of various categories of aquatic able to attribute to biological processes a dom- ecosystem. It moves on to examine the responses inant contribution in the contemporary carbon of pelagic systems to changes, especially those cycle. wrought through deliberate and unthinking Just as certainly, they will also impose a bal- anthropogenic activities. anced distribution of the contemporary anthro- In the open water of the sea and of the largest pogenic contribution to carbon dioxide ‘inhala- lakes (those >500 km2 in area), phytoplankton tion’ by the sea. This being a warm (and warming) are the only photoautotrophic primary produc- phase, the rate of inhalation may be less rapid ers, upon which everything else in the water is than during a glacial phase. On the other hand, dependent for its nutrition (energy as fixed car- the flooding of coastal plains rich in nutrients bon and the other elements of biomass). This may accelerate carbon withdrawal into diatoms long-standing view is correct but the secondary and other ‘large’ phytoplankters. Moreover, the processing of primary product depends less on rate of exploitation of the finite and increas- thegrazing of phytoplankton, as once supposed, ingly inaccessible remnants of the fossil-fuel car- so much as on the microbial uptake of fixed carbon is, in any case, bound to diminish, so the bon released into the medium by the producers. fluxes from atmosphere to ocean will, inevitably, Severe poverty of nutrient resources controls the reduce. Within the context of the last 100 Ma, the biomass at all trophic levels but carbon contin- present carbon crisis would seem relatively trivial ues to be traded through the food-web compo- and unlikely to disturb the pattern of prokaryote- nents. The bacteria → nanoflagellate → ciliate mediated carbon cycling in the open ocean and → copepod pathway delivers efficiently a yield, eukaryote-mediated exports from shelf waters. perhaps nearly 10% of the original primary prod- The pre-industrial quasi-steady state might be uct. A further 10–20%, up to 100 mg C m−2 a−1, re-established within 100–200 years and, if not, may be exported by sedimentation. The balance before the onset of the next glacial phase. of the carbon budget is simply recycled through It is prudent, nevertheless, to follow my own thepelagic network, which thus constitutes a stricture and recognise the weak base for ‘reli- fairly closed cycle. The export is argued to be sim- able and precise anticipation’. Nobody can be ilar in magnitude to the net annual invasion of sure that the rate of global warming will not atmospheric carbon. The system is a quasi-steady SUMMARY 433 state, a low, stable, average biomass being run on ter feed) are geared to the availability of their theavailable flux of carbon. The activity is analo- nutritional requirements. The corollary is that gised to a small wheel spinning rather fast (20 to therelatively most abundant forms will be those 70 revolutions per year, according to the criteria most capable of fulfilling their requirements. used). This is another way of saying that species compo- In the pelagic zones of smaller lakes, coastal sition (at least at the level of functional types) seas, shelf waters and upwelling areas of the depends, in part, on the resource base. For ocean, primary production benefits from addi- example, greater nutrient availability raises the tional supplies of inorganic carbon, including autotrophic supportive capacity, enabling pho- that dissolved in inflowing streams and rivers toautotrophic phytoplankton to retain more of and the metabolic gases released through the their own photosynthate in their own biomass, oxidation of sedimentary organic carbon. The and with a lesser proportion garnered by het- delivery to the water-body margins of terres- erotrophic plankton. Greater nutrient availability trial particulate organic carbon can provide a makes it easier for larger species of algae to flour- direct input to littoral and sub-littoral consump- ish in the pelagic. Mesozooplanktic feeding on tion. The interaction with the adjacent terrestrial absolutely larger nano- and microplanktic algal ecosystems contributes to enhanced fixation of fractions short-circuit the microbial web; filter- inorganic carbon (net yields of primary produc- feeding zooplankton are capable of its destruction range are frequently in the range 200–800 g tion. The optimal pelagic pathway changes to Cm−2)aswell as providing an additional income microalgae → cladoceran. of organic carbon to limnetic heterotrophs. The How the pelagic community processes its shallow littoral margins of lakes are important in resources and directs the flow of energy is shown other ways, not least because of their ability to to be strongly conditioned by the activities of the support macrophytic plant production. Stands of main species (that is, how the community func- aquatic plants accumulate organic debris (some tions is a consequence of what is there). Exam- of it by filtration from the circulation), offer shel- ples are presented that show that the princi- terand microhabitats to invertebrates. Linked to pal components of the phytoplankton and zoo- thepelagic through the horizontal movements of plankton, as well as the foraging activities of animals, especially fish, macrophyte stands influ- fish, can be matched to the carbon concentration ence the material and energy flow to a consider- (subsidised or otherwise) and the energy trans- able distance into the lake. The additional car- ferred among trophic levels. Critical boundaries bon flux represents a supportive subsidy with of ∼0.01 mmol C L−1 (∼0.12 mgCL−1)distin- respect to the truly pelagic system. The smaller guish classically eutrophic lakes from classically is the water body then the relatively greater is oligotrophic lakes. A similar abundance of car- the potential subsidy to the overall function of bon separates those lakes that support Cyanobac- the lake. More carbon, proportionately and abso- teria from those in which chrysophytes are abun- lutely, may reside in the biomass of aquatic pro- dant; those whose zooplankton is dominated ducers, phagotrophic consumers and other het- by calanoids from those in which cladocerans erotrophs of smaller lakes and ponds, provided are abundant; and those supporting coregonids always that it is within the stoichiometric capac- from those in which benthivorous fish dominate. ity of the limiting bioavailable nutrient(s). It is also suggested that, in small to medium- Resource availability and processing con- sized lakes where the carbon balance exceeds this straints determine the relationship between threshold, a large, possibly dominant, part of the energy flow and the structure (sensu the func- authochthonous organic carbon is transmitted to tional groupings of the main participants). The higher trophic levels by way of the sub-littoral abilities of phytoplankton to gather resources sediments, benthic invertebrates and browsing (whether through diffuse demand, high uptake benthivorous fish. affinities or scavenging propensity) and of zoo- The chapter also considers the suscepti- plankton to forage (to encounter, to hunt, to fil- bility and dimensions of changes in pelagic 434 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

communities consequential upon anthropogenic ing of the shorelines are unwelcome symptoms of changes. Eutrophication of lakes through enhan- eutrophication. Phytoplankton abundance preju- ced phosphorus loading is considered in some dicial to water quality, to treatment for potability detail, developing the underlying processes link- and to the quality of fishing is likely to inspire ing catchment sources (‘loads’) of phospho- and justify the costs of reversal of eutrophica- rus to in-lake concentrations and the mean tion (‘oligotrophication’), and the restoration of algal biomass (as chlorophyll a concentration) past quality or rehabilitation of the water body in the lake, as represented in the well-known to an acceptable ecological state. A series of suc- Vollenweider–OECD regression. cessful schemes in which phosphorus-load reduc- The relationship remains a powerful descriptions have led to reduced plankton biomass and tor ofthebiomass capacity of the deep, high- better perceived water quality is highlighted. The latitude lakes that dominated the original biological response is usually dramatic but it dataset, but it is not a general management is never manifest before the soluble, MRP frac- model. Mean phytoplankton abundance in low- tions, readily available to support further phy- latitude lakes, in shallow lakes, especially those toplankton growth, are effectively drawn down experiencing fast rates of hydraulic exchange, to thelimits of detection. Phosphorus-reduction and those in which phosphorus is manifestly not schemes that, so far, have been unsuccessful in the capacity-regulating factor, is not well simu- invoking the desired biomass response have not lated by the regression. Special problems aris- achieved, or have progressed too slowly towards, ing from the abundance of particular types of thesatisfaction of this criterion. These poor phytoplankton are considered here. Even though responses are observed frequently among shallow their dominance may have only tenuous connec- lakes, where the persistent recycling of phospho- tions with nutrient eutrophication, their abun- rusfrom already enriched sediments goes on sus- dance is potentially greater where there is signifi- taining phytoplankton independently of external cant enrichment. Conspicuous among the organ- loads. isms generating nuisance on aesthetic grounds Methods for anticipating the sensitivity of are the bloom-forming Cyanobacteria. These have individual sites to altered external loadings (up the added hazard of often being highly toxic. as well as down) are available. If control over They are difficult to eradicate from lakes but, the internal loads (or adequate contol over the with an understanding of their preferences and external loads) is impractical, other rehabilitative weaknesses, some kinds of lake and reservoir can approaches are available. Provided the water col- be managed in ways that keep these algae in umn is deep enough to make a difference, arti- check. Cyanobacterial blooms are not confined to ficial circulation of water bodies (chiefly reser- inland waters, having become common in recent voirs) to break or to prevent thermal stratifi- years intheBaltic Sea. Elsewhere, harmful algal cation reduces the light-carrying capacity and blooms in the sea comprise ‘brown tides’ of Aureo- rates ofgrowthofphytoplankton. Subject to the coccus,‘greentides’ofPhaeocystis and, especially, same provision, the overriding imposition of defi- ‘red tides’ of toxic dinoflagellates. In all events, cient insolation pushes species composition in local abundances may depend upon concentra- favour of functional types with acknowledged tion by water movements but the incidence of light-harvesting specialisms (diatoms, filamen- such events is increasing and are considered tous green, yellow-green and blue-green algae, indicative of nutrient enrichment of the shelf of trait-separated groups P, T and, especially, S). waters from which they are best known. Several examples are presented where mixing There are few instances where eutrophication of deep reservoirs assures reasonable supplies of is considered beneficial; mostly it is abhorred on waterfor treatment and within predictable lim- aesthetic grounds of appearance, the detriment its of phytoplankton abundance. usually being directly attributable to increased There is a good prospect of restoring or reha- biomass of phytoplankton and littoral epiliths. bilitating those ‘small’ lakes (i.e. up to 10 km2 Greening of the water, loss of clarity and sully- in area) and, especially, ‘shallow’ lakes (in which A LAST WORD 435

>50% of the area is <5mindepth) through <2.5. The problem of metal (Al, Zn, Cu) toxicity the biomanipulation of the ecosystem compo- is generally critical. nents. Investment of carrying capacity is moved Apart from some estuaries, coastal waters from phytoplankton to macrophyte and/or fish and part-landlocked shelf areas, the open seas biomass. The necessary changes in the consump- have suffered less from anthropogenic nutrient tion pressures may be imposed from the top enrichment than from severe food-web distor- down by adjusting the abundance of fish pop- tions as a consequence of exploitative industrial ulation (lower the density of planktivores, raise fisheries. Indeed, deliberate fertilisation of the thedensity of piscivores; both supposedly reduce oceans, with a view to increasing carbon fluxes the controls on zooplankton which, obligingly, from atmosphere to sea water, has been seriously graze down the phytoplankton). Managers still suggested as a counter to the net accumulation find themselves having to repeat treatments to of greenhouse gases from the oxidation of fos- enforce the imposed, non-steady state. Left to sil fuels. Such action is argued to be misguided. themselves, water bodies will often gravitate to While the carbon storage capacity of the ocean asystemcharacterised by high POC/dissolved is not exhausted, the net carbon flux is possibly nutrient concentrations → Planktothrix agardhii as fast as it can be. If fertilisation could secure → chironomids → cyprinids. The task is to therapid deep transport of POC (for instance, induce the system into a valid alternative, macro- in diatoms or faecal pellets) balances might be phyte → benthos → fish, steady state, in which altered a little. Possible outcomes are consid- better habitat and water quality are more nearly ered. The consequences for human societies are self-maintaining. Even here, there are approxi- uncomfortable to contemplate. mate critical boundaries (in terms of phosphorus rather than carbon). These may not be easy to pass in the downward direction, usually requir- 8.5 A last word ing quite drastic interventions into the numbers of planktivorous and benthivorous fish. Below On the time and space scales of the biogeochem- the critical boundaries, however, handbook guid- istry of the Earth, the current ‘carbon crisis’ is ance extols the importance of macrophyte domi- modest, and more serious shifts in the planetary nance to attractive ecosystems. Put simply, macro- distribution of carbon have occurred in the Meso- phyte beds support macroinvertebrate popula- zoic. Indeed, the groups of phytoplankton that tions adequate to interest many species of adult evolved during that era – diatoms, dinoflagellates fish, and a sufficient refuge for cladocerans to and coccolithophorids – may have done so in keep the water reasonably clear of phytoplank- response to contemporaneous ocean–atmosphere ton. The boundary (‘switch’) in the upward direc- interactions, have persisted for 100 million years tion is mediated by the algal biomass spon- and may still be best equipped to operate through sored by bioavailable phosphorus concentrations theworst anthropogenically induced changes exceeding 120–180 µgPL−1, whether it is present that can be anticipated. as phytoplankton or epiphytic growth. Further It is perhaps humbling that precise extrapola- stability may be brought by stocking with pisci- tions cannot be made. Through the past century vores suchaspike. and a half, there have been several reasons for Brief consideration is directed towards the studying phytoplankton, not least for the beauty selective responses of phytoplankton to anthro- (that first attracted Haeckel), the desire to cata- pogenic acidification. The impacts on some logue and name many thousands of species and waters affected by acid precipitation are cata- thechallenge of sorting out their phylogenetic logued. However, in this instance, algal behaviour affinities and evolutionary development. These in highly acidic waters filling some Lusatian min- persist today. The physiology of cell growth and ing hollows and a natural, sulphate-rich caldera replication and collective impacts in the global in Argentina illustrate the remarkable tolerances carbon and oxygen cycles represent extremes of of a few green-algal species down to pH values of a scale covering a dozen orders of magnitude and 436 PHYTOPLANKTON ECOLOGY AND AQUATIC ECOSYSTEMS

nearly as many biological disciplines. The ecology somes are providing ever greater dimensions of of populations and communities is relevant to precision to the knowledge base. Yet it is quite many aspects of human existence, from the safety evident that, far from knowing all there is to of drinking water to the sustainability of ﬁsh- know about phytoplankton, relevant and polit- eries. The accumulated knowledge is both broad ically sensitive questions persist, such as pre- and deep but it is far from complete. Common dicting and understanding the impacts of global tenets and basic understanding of the pelagic warming on the fundamental life-supporting sys- ecosystem have undergone comprehensive revi- tems of the planet. The answers elude us. Much sion more than once, the most recent occasion needs to be done; the scientiﬁc study of phyto- having been only in the last two decades. Com- plankton will continue. Tomorrow’s leaders need pletely new organisms and new organisations are an appreciation of the breadth and limits of exist- being found, even now, in the deep oceans and ing knowledge of our home planet. It is my fer- in the vicinity of hydrothermal vents. New tools, vent hope that this book may contribute to the from satellite-based remote sensing to the anal- base of reference and the stimulus for the future ysis of gene sequences from individual chromo- research. Glossary

Text boxes are used to explain the usage of certain terms specific to plankton (Box 1.1)andtheir ecology (Box 7.3). The meanings of some other less familiar terms used in the book are noted below. abyssal pertaining to the abyss, or the very deep parts chemotrophy the capacity of organisms to obtain of the ocean energy through chemical oxidation and using aeolian of the wind, referring to the transport and either inorganic compounds as electron donors deposition of dust particles from the land to lakes (chemolithotrophs) or preformed organic and oceans compounds (chemoorganotrophs) amictic of lakes that are scarcely wind mixed or chromophore intracellular organelle containing which are weakly and incompletely mixed for very photosynthetic pigments long periods coccoliths flattened, often delicately fenestrated anoxygenic photosynthesis carbon fixation that takes scales, impregnated with calcium carbonate place in the absence of oxygen and during which coenobium (plural coenobia)agroup of monospecific no oxygen is produced; photosynthesis that does cells forming a single, often distinctive unit not split water to generate oxygen compensation point the point in a water column at atelomictic of water columns, usually in low latitudes, which the rate of photosynthesis of an alga just in which the depth of wind mixing varies balances its respiration; or the notional point when conspicuously in extent but at frequencies the daily depth-integrated photosynthesis of days to weeks rather than at diel or annual compensates the daily depth integral of respiration cycles dimictic of lakes and water bodies, generally at mid autotrophy the capacity of organisms to grow and to high latitudes, that are fully mixed during two reproduce independently of an external supply of separate periods of the year (typically spring and organic carbon; the ability to generate organic autumn) carbon by reduction of inorganic sources using emergy the total amount of energy required to light or chemical energy produce the usable energy of a final product. In the auxospore sexually reproduced propagule of diatoms ecological context, a grown elephant contains that also enables organismic size to be recovered biomass equivalent to a potential yield of direct after a period of asexual replication energy but a lot more energy has been lost in bathypelagic of the deep open water of the ocean foraging for food, as well as in its production benthic of the solid surfaces at the physical bottom Emergy represents the sum of these contributions of aquatic habitats; this can be very shallow as well endosymbiosis asymbiosis between two organisms in as far beneath the water surface which one lives entirely within the body of the bioassay atechnique for identifying the supportive other but to the mutual benefit of both partners capacity of water and for identifying nutritive epilimnion the upper part of a seasonally stratified components that are deficient therein; if the lake; the part between the water surface and the addition of a particular nutrient raises the response first seasonal pycnocline relative to the unmodified control then that eukaryote acellular organism having a nutrient is deemed to have been limiting the full membrane-bound nucleus within which the response chromosomes are carried biogenic of the ability of living materials to create or euphotic zone that (upper) part of the water column generate a particular substance; of substances thus wherein there is sufficient light to support net generated bylivingorganisms photosynthetic gain (often approximated as cadavers the corpses and remains of dead organisms requiring 1% of surface light intensity but, in carboxylation the essential step in photosynthesis reality, variable according to species and light involving the combination of carbon dioxide, water history) and ribulose biphosphate and yielding the initial exergy the extent of high-quality, short-wave energy fixation product that incorporates the high-energy that an individual, population or community can phosphate bond invest in the synthesis of biomass (see also Box 7.3) 438 GLOSSARY

form resistance theresistance to movement through mixis wind- or convection-driven integration of the water effectedbyshape distortion with respect to a water massesofalake;complete mixing is called sphere of similar volume and density holomictic;frequentcomplete mixing is described as frustule the siliceeous case of a diatom, comprising polymictic two similar valves mixolimnion the upper part of a meromictic lake; the haptonema distinctive additional appendage, said to part between the water surface and the perennial be characteristic of the Haptophyta, carried pycnocline, that is actually or potentially mixed anteriorally, between the flagella during the year heterocysts (or heterocytes) specialised cells of mixotrophy the capacity of an autotroph to Cyanobacteria (Nostocales) dedicated to the fixation supplement its carbon and/or nutrient requirement of nitrogen (see Fig. 1.4h) from externally produced organic carbon heterotrophy the means of nutrition of organisms compounds that grow and reproduce that is dependent upon neritic pertaining to the shallow, inshore regions of externally produced organic carbon compounds as the sea asource of carbon and energy osmotrophy the capacity of certain microorganisms to hypolimnion the lower part of a seasonally stratified absorb selected dissolved organic compounds across lake; the part between the seasonal pycnocline and the cellsurface thelake floor oxidation chemical reaction involving the removal of isopycny the condition of one entity having the same electrons and/or hydrogen atoms with, usually, a density as another or as the medium in which it is release of energy suspended phagotrophy case of heterotrophy in which organic karyokinesis the apportionment of the mitotically carbon is ingested in the form of another organism reproduced genetic material of a cell; nuclear or part thereof, requiring digestion prior to division assimilation kataglacial of processes or deposits associated with photoautotrophy autotrophy using light energy to the melting of glaciers generate organic carbon by reduction of inorganic kinase an enzyme that mediates the transfer of sources phosphate groups from (e.g.) ATP to a specific phycobilin accessory biliprotein pigment of substrate or target molecule Cyanobacteria, also found in Rhodophyta, some laminar flow ordered fluid motion, molecules cryptophytes and glaucophytes moving in layers, one upon another prokaryote cellular organism lacking lorica hard part of the surface of certain flagellates, membrane-bound nucleus and organelles especially euglenophytes and chrysophytes; from phytoplanktont or phytoplankter terms applied to an the Latin word for breastplate individual organism of the phytoplankton meromixis condition of (usually) deep tropical lakes in pseudotissue tissue-like structure of a fungus but which mixing energy is inadequate to overcome comprising hyphae in close mutual application stratification and which, therefore, remain pycnocline agradient (usually vertical) separating stratified for many years on end water massesofdifferent densities. The density meroplankton organisms that are planktic for a short difference may be due to a difference in part of their life history, the rest of which they pass temperature or solute (e.g. salt) content in the benthos or in the periphyton reduction chemical reaction involving the addition of metalimnion the intermediate part of the water electrons and/or hydrogen atoms with, usually, an column, separating epilimnion and hypolimnion investment of energy; the opposite of and characterised by density gradients and much oxidation weaker vertical diffusivity than either of the layers redox potential the balance of electrochemical it separates potential between oxidative and reducing reactants monomictic of lakes and water bodies, generally at reductant chemical substance that will yield low to mid latitudes that are fully mixed during electrons and hydrogen ions only one part of the year (typically between solar constant the energy flux from the Sun to the autumn and spring) Earth, estimated as that reaching a notional surface monimolimnion the lower part of a meromictic lake, held perpendicular to the solar rays and at a point between the perennial pycnocline and the lake floor above Earth’s atmosphere, before there is any GLOSSARY 439

reﬂection, absorption or consumption. It is not tychoplankton organisms that are not planktic constant but an average, about 1.36 kW m−2 but which may, fortuitously, be introduced thermocline agradient (usually vertical) separating to the plankton from adjacent habitats. The watermasses of different temperature distinction from meroplankton is narrow but thylakoid membrane supporting the light-harvesting the criterion is whether the suspended complexes and sites of phase is essential to the life cycle or purely photosynthesis incidental Units, symbols and abbreviations

UNITS

Dimension Unit Notation Equivalent mass kilogram kg gram g10−3 kg gram molecule mol length metre m area square metre m2 volume cubic metre m3 litre L 10−3 m3 density kilogram per cubic metre kg m−3 time second s day d 86 400 s year a velocity metres per second m s−1 acceleration metres per second per ms−2 second force newton N kg m s−2 pressure pascal Pa N m−2 = kg m−1 s−2 viscosity poise P N m−2 s−1 = kg m−1 s−1 work joule J N m = kg m2 s−2 power watt W J s−1 absolute temperature kelvin K customary temperture degree Celsius ◦CK+ 273 Arrhenius temperature reciprocal Kelvin A 1000/K electrical potential volt V molecular weight dalton Da concentration mass per volume, e.g. kg m−3 M mol L−1

Multiple units Symbols

Many units are managed numerically by the use Areciprocal kelvins × 1000 of preﬁxes, as in Pg (for petagrams), µm(for Da molecular weight, especially of large micrometres) or nM (for nanomols L−1). The SI molecules notations are used throughout: P = 1015 times Eq equivalent mass of a reactant ion or the basic unit; T = 1012;G = 109;M = 106;k(or substance K) = 103;m = 10−3; µ = 10−6;n = 10−9; p = Jjoule, the basic unit for expressing work 10−12;a = 10−15. Kkelvin, the basic unit for expressing absolute temperature UNITS, SYMBOLS AND ABBREVIATIONS 441

Llitre,acustomary unit of volume; 1 m3 = D demand for a resource 1000 L Dx coefficient of horizontal diffusivity Mmolar, being a concentration of 1 gram (see Eq. 2.37) − molecule per litre of solvent (herein, E rate of energy dissipation, in m2 s 3 always water) Es equitability or eveness of species Nnewton,thebasic unit for expressing representation in a multi-species force community Nnitrogen Fa solute flux to the vicinity of a cell Ppoise,the basic unit for expressing (see Eq. 4.4) viscosity FC flux of CO2 across the water surface, − − Pphosphorus in mol m 2 s 1 (see Eq. 3.18) [P]i phosphorus concentration of the ith Fi filtration rate (sensu volume processed inflow stream to a receiving water per unit time) of an individual Pa pascal, the basic unit for expressing filter-feeding zooplankter pressure F0 emitted chlorophyll fluorescence, Vvolt, the basic unit for expressing electric when all light-harvesting centres are potential open, compared to the fluorescence ayear following a subsequent saturating dday flash (Fm) d (as a prefix) indicating a very small Fm emitted chlorophyll fluorescence, increment, as in: when all light-harvesting centres dN population rise are closed by a saturating flash of dt time increment light = − dSe extrabiotic dissipative flux of solar Fv variable fluorescence ( Fm F0), energy G material removed by consumers from dSi biotic dissipative energy flux agivenvolume and in a given time ethe base of natural logarithms period ggram GC the gas exchange coefficient, or linear − ln natural logarithm (i.e. power to base e) migration rate m s 1 (see Eq. 3.18) log standard logarithm (i.e. power to base 10) H the depth of water in a flow or lake mmetre H Shannon diversity in bits I irradiance, or the flux of visible light pCO2 the partial pressure exerted by atmospheric gaseous carbon dioxide (or PAR), or photon flux density, in ssecond mol per unit area per unit time I0 instantaneous irradiance flux penetrating the surface of the sea or a Variables lake, usually expressed in µmol photon m−2 s−1 or integrated over the A adefined area of the Earth’s surface day as mol photon m−2 d−1 Ax the cross-sectional area of a river Ic notation for the intercept of channel (in m2) photosynthetic rates (P) against (I) B biomass derived in Fig. 3.3 Bmax biomass-supportive capacity of the Ik irradiance intensity that just saturates available resources or, effectively, the photosynthetic rate maximum biomass that can be Im residual irradiance intensity at the supported by the available resources base of the contemporary mixed layer BQ energy of penetrative convection IP=R irradiance intensity that sustains just Co solute concentration, as in Fick’s enough photosynthesis to meet equation (3.19). respirational demand, and which 442 UNITS, SYMBOLS AND ABBREVIATIONS

defines the water-column N population of particles or organisms compensation point or their biomass per unit area or Iz irradiance intensity at a given depth volume (as specified) in the water column, z N0 initial population, N (i.e. at t = 0) and I530 irradiance intensity at the subscripted subject to dynamic change wavelength Nt population remaining after a period I∗ instantaneous integral of fluctuating of time, t, has elapsed irradiance intensities applying in a Nt/m specifically to settling particles, to mixed layer show an alternative outcome at t, had I∗∗ integral of fluctuating irradiance thesettlement been subject to m intensities applying in a mixed layer complete and instantaneous mixings over the day NP communal photosynthetic rate, being Jb buoyancy force in the surface mixed theproduct of the chlorophyll-specific layer, owing to the difference in its photosynthetic rate (P) and the density with that of the water population, as chlorophyll, present (N) immediately beneath P individual, usually biomass-specific, Jk the kinetic energy available to photosynthetic rate, expressed by overcome buoyancy of the surface mass of carbon fixed or oxygen mixed layer generated per unit biomass carbon or Ki Steady-state concentration of the ith chlorophyll per unit time nutrient resource P primary production Kr half-saturation constant of Pg gross primary production resource-limited growth rate (i.e. the Pn net primary production concentration of resource at which Pmax maximum observed or extrapolated therate of cell replication, r,ishalf photosynthetic rate the maximum when growth rate PQ photosynthetic quotient, as mol O2 uptake is nutrient-saturated) evolved per mol CO2 assimilated KU half-saturation constant of resource Pe Péclet number, being the ratio of the uptake (i.e. the concentration of momentum of a moving particle to resource at which the rate of diffusive transport in the medium uptake, VU,ishalfthemaximum Q s short-wave solar radiation when uptake is nutrient-saturated Q T net radiative heat flux reaching the −2 (VUmax ) planetary surface (units, W m or J L Horizontal downwind distance over m−2 d−1) ∗ alakeorotherdefined water Q T that fraction of Q T that penetrates body beyond the top millimeter or so of LD ‘light divisions’; Talling’s (1957c) thewater column integral of light intensity in a water Qz net radiative heat flux reaching a column capable of supporting net given point in the water column photosynthesis: LD = [ln (I 0max/ 0.5 Ik) R rate of respiration (or biomass /ln2] maintenance) LDH Talling’s (1957c) ‘light division hours’, Ra rate of community respiration expressing the daily integral contributed by photoautotrophs ◦ irradiance received by a water body Ra20 steady Ra at 20 C that is deemed to support Rh rate of respiration of heterotrophs phtosynthesis (see Eq. 3.20) Re Reynolds number, being the ratio L(P) aggregate areal rate of phosphorus between the driving forces of water loading to a lake (in mg m−2 of lake flow and the viscous forces resisting area per year) them UNITS, SYMBOLS AND ABBREVIATIONS 443

Rib bulk Richardson number, being the hw height of a theoretically static water ratio between the driving forces of layer motion in a water body and the i,j identifiers in a multiple component buoyant resistance to entrainment of list of variables deep waters k exponential coefficient of heat S supply or concentration of a resource absorption (see Eq. 2.27) Sh Sherwood number, being the ratio k exponent of invasiveness of dispersing between the total flux of a nutrient organisms (see Eq. 7.3) solute arriving at the surface of a cell ka area-specific light interception of an in motion and the wholly diffusive alga flux kn rate of population change in a U wind velocity horizontal patch (see Eq. 2.37) Vvolume of a lake or other defined la length dimension available for the body of water dissipation of the energy, usually the VU rate of uptake of a given nutrient depth of the flowing water layer

VUmax nutrient-saturated uptake rate of a le length dimension of the largest given nutrient turbulent eddies W Wedderburn number, being the ratio lm smallest eddy size supported by the between the Richardson number of a available mechanical energy before structure and its aspect ratio (see it is overwhelmed by viscous Eq. 2.34) forces Wb dry mass of a zooplankter m number of mixing events Wc dry mass of an algal cell (Section 2.6.2) a factor of increased diameter, used in m maximum cell dimension Eq. (2.17) m maximum size of particle that is a area term used in Fick’s equation available to a given filter-feeder (3.19) n number of moles of a solute that will b number of beads in a chain as a diffuse across an area variable in sinking rate (see Eq. 2.18) n(t) number of exploitable niches in the bi biomass of the ith of s species present location at a time t in a community or sample ñ number of occupied niches when c speed of light t =∞ cd coefficient of frictional drag nsp number of species to be found in a d diameter of a spherical cell defined area, A,asinfluenced by dc diameter of a cylindrical cell arrivals and extinction rates ds diameter of a sphere of equal volume p wetted perimeter of a vertical to an irregularly shaped particle section through a stream g gravitational acceleration (here taken channel as a constant 9.8081 m s−2) q cell-specific content of a given h Planck’s constant, having the value nutrient (or quota) (see Eq. 4.12) −34 6.63 × 10 Js q0 minimum cell quota of a given hc height of a cylidrical cell nutrient, below which it is deemed to hm height of the mixed layer, from its be no longer viable base to the water surface qmax replete cell content of a given hp height of the photic layer, being from nutrient the depth of IP=R to the water surface qi the inflow rate, or inflow volume per hs height of the water layer from the unit time (usually) to a lake surface to the depth of Secchi-disk qs discharge, or outflow volume per unit extinction (zs) time (usually) from a lake 444 UNITS, SYMBOLS AND ABBREVIATIONS

r exponent of therateofcell tq theoretical hydraulic retention time replication, or rate of cell recruitment (V/qs) through growth tw measured hydraulic retention time r max resource-saturated rate of cell (V/qs) replication u vector or flow velocity in the r 20 rate of cell replication at temperature horizontal (x) plane 20 ◦C u¯ mean horizontal velocity of turbulent r θ rate of cell replication at the field flow temperature θ ± u velocity variations in turbulent flow r θ,I rate of cell replication at the field in relation to u¯ temperature θ and the natural light us horizontal advective velocity around conditions patch ∗ r (Si) rate of cell replication of diatoms u turbulent velocity, the friction calculated from uptake of soluble velocity or the shear velocity, as reactive silicon from solution derived in Section 2.3.2 and Eq. (2.4) ∗ 2 rc critical radius of a patch able to (u ) turbulent intensity, as derived in maintain distinctive pelagic Section 2.3.2 populations (see Eq. 2.37) uˆ arrival rate of colonist species at a rp roughness of the stream bed given habitat (sensu the height of projections) v volume of a phytoplankton cell or (see Eq. 2.6) colony rn exponent of the rateofincreaseofa w vector or flow velocity in the vertical self-replicating population net of (z) plane simultaneous rates of loss ± w velocity variations in turbulent flow rL sum of the exponents detracting from in the vertical direction aself-replicating population wc sinking rate of chain rG exponent of the rate oflossfroma ws sinking rate of algal cell or colony population of cells to consumers wP rate of loss of phosphorus in the rS exponent of the rate oflossfroma outflow from a lake population of cells to settlement x concentration of organisms in a rW exponent of the rate oflossfroma sample, used in the calculation of population of cells to wash-out Lloyd’s crowding index (see Sections s surface area of a cell or colony 2.7.1 and 2.7.2) −1 sb gradient of the stream bed (in m m ) x¯ mean of concentration, x,inaseries s2 statistical variance of samples t aperiod of time or a fixed point in x∗ Lloyd’s crowding index, based upon time the variance in x among individual t ashorterperiodoftimewithint or samples. The greater the variance, the an intermediate fixed point greater is the difference among tc limiting closure period of LHC individual samples. In Sections 2.7.1 intercepting light (in s photon−1) and 2.7.2,theindex is used to gauge te time to achieve total elimination (or a theeffect of wind upon small-scale defined proportion) of particles from patchiness suspension z used to identify points in the vertical tm probabilistic time of travel of an direction; a specific depth

entrained particle through a mixed z(Ik) depth beneath the water surface at layer which Ik is located; depth below tp photoperiod or time spent in which photosynthetic rate becomes euphotic zone light-dependent UNITS, SYMBOLS AND ABBREVIATIONS 445

γ z(0.5I k ) depth beneath the water surface at temperature coefficient of thermal which photosynthetic rate is 50% that expansion, given by − (1/ρw) (dρw / at light saturation dθ)K−1 zeu the depth of the conventionally δ to indicate ‘increment in’ defined euphotic layer ε exponent of vertical light attenuation −1 zm the depth to which the water is in water (units, m ) mixed; the base of the mixed layer εa exponent of that part of the vertical zs theSecchi-disk depth, being the light attenuation due to the presence distance beneath the surface at which of planktic algae aSecchidiskbecomes obscured from εp exponent of that part of the vertical the observer above the water surface light attenuation due to the presence (see Box 4.1) of tripton day length from sunrise to sunset εw exponent of that part of the vertical to indicate difference, as in ρw (of light attenuation due to absorption by density between top and bottom the water waterinastratified water body) εz exponent of vertical light attenuation N integral of simultaneous at a given depth concentration gradients (δ/δx, δ/δy, ε440, ε530,exponent of attenuation at the δ/δz)inthex, y and z planes (nabla etc. particular wavelengths operator) (see Section 4.2.1) εmin coefficient of attenuation in P mean availability of phosphorus in a least-absorbed waveband lake taking account of loading and εav coefficient of attenuation averaged hydraulic exchanges overanumber of wavebands w to indicate ‘sum of’, as in Fi, the εav is a weighted average attenuation cumulative filtration rate of coefficient average (see Section 3.3.3) filter-feeders in a unit volume of ε the energyofasingle photon; ε medium, and tp varies with the wavelength (= hp / hm),thedaily sum of (see Eq. 3.2) photoperiods η absolute viscosity of a fluid, NP area-integrated photosynthetic rate, in kg m−1 s−1 expressed as the sum of NP ν kinematic viscosity of a fluid, NP daily area-integrated photosynthetic in m2 s−1 rate θ temperature, usually in ◦C NR area-integrated respiration rate, λ wavelength (e.g. of light, in nm) expressed as the sum of NR ξ gas solubility coefficient (in mol m−3 NR daily area-integrated respiration rate atmosphere−1) quotient relating sinking behaviour to π the ratio of the circumference of a turbulent diffusivity, used as an index circle to its diameter of entrainment (explained in Section ρ density, usually in kg m−3 2.6.1) ρa density of air α coefficient of slope of a regression of ρc density of a cell y on x,usedhereinmainlytodescribe ρm density of mucilage −3 light dependence of photosynthesis ρw density of water, in kg m and growth (α = P/I) σ specific heat of water, in J kg−1 K−1 αr growth efficiency on low light σ s succession rate index incomes, derived from the slope of σ P phosphorus sedimentation rate the regression of r on I σ X cross-sectional area of a β slope of maximum replication rate on light-harvesting centre Arrhenius temperature scale τ force orstress, in N 446 UNITS, SYMBOLS AND ABBREVIATIONS

ϕ quantum yield of photosynthesis, in HNF heterotrophic nanoflagellates mol C (mol photon)−1 IDH intermediate disturbance hypothesis ϕr coefficient of form resistance LAIleaf area index (dimensionless) LHC light-harvesting complex ω coefficient of selectivity of ingestible MLD maximum linear dimension particles from the inhalant current of MPF maturation-promoting factor (see afilter-feeder Section 5.2.1) 0 integral sign, as in ∞:integrate MRP molybdate-reactive phosphorus from zero to infinity, or to a large NADP nicotinamide adenine dinucleotide number phosphate NAO North Atlantic Oscillation NPP net primary production Abbreviations used in the text NTA nitrilotriacetic acid OECD Organisation for Economic APhoton acceptor for photochemical Co-Operation and Development system I PARphotosynthetically active radiation ANN artificial neural network PCR polymerase chain reaction APAR absorbed photosynthetically active POC particulate organic carbon radiation POM particulate organic matter ATP adenosine triphosphate POOZ permanently open-ocean zone (of BAP biologically available phosphorus high-latitude waters) BOD biochemical oxygen demand PP particulate phosphorus CCM carbon-concentration mechanism PQ plastoquinone CRP cAMP receptor proteins PSI photochemical system I CV coefficient of interannual variation PSII photochemical system II DAPI 4,6-diamidino-2-phenylindole (see QA,QB quinones in PSII Section 5.5.1) RNA ribonucleic acid DCM deep chlorophyll maximum RUBISCO ribulose 1,5-biphosphate carboxylase DCMU 3-(3,4-dichlorophenyl)-1, 1-dimethyl RuBP ribulose 1, 5-biphospate urea SEH size-efficiency hypothesis DEU dissipative ecological unit SIZ seasonally ice-covered zone (of DHM dissolved humic matter high-latitude seas) DIC dissolved inorganic carbon SRP soluble reactive phosphorus DIN dissolved inorganic nitrogen SRSi soluble reactive silicon (combined; does not include STPP sodium tripolyphosphate dissolved nitrogen gas) TFe total iron (sensu all chemical forms DMS dimethyl sulphide present) DMSP dimethyl-sulphonioproponiate TN total nitrogen (sensu all chemical DNA deoxyribonucleic acid forms present) DOC dissolved organic carbon TP total phosphorus (sensu all chemical DOFe dissolved organic iron (complexed forms present) with DOC) a.s.l above sea level DON dissolved organic nitrogen cAMP cyclic adenosine monophosphate EDTA ethylene diamine tetra-acetic acid chla chlorophyll a FDC frequency of dividing cells [chla] concentration of chlorophyll a GPP gross primary production [chla]max maximum supportable concentration G3P glycerate 3-phosphate of chlorophyll a G3AP glyceraldehyde 3-phosphate ppGpp guanosine 3,5-bipyrophosphate HAB harmful algal bloom tris trishydroxymethyl-aminomethane References

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LAKES AND Carrilaufquen Chica, Argentina Garda, Lago di, Italy 45◦ 35 N, RESERVOIRS 41◦ 13 S, 69◦ 26 W 335 10◦ 25 E 330, 331 Table 7.4 Carrilaufquen Grande, Argentina George, Lake, Uganda 0◦ 0 N, ◦ ◦ ◦ ◦ 41 7 S, 69 28 W 335 30 10 E 59, 105, 344 Akan-Panke, Japan 43 27 N, ◦ ◦ ◦ Castle Lake, California, USA Grasmere, UK 54 28 N, 3 1 W 241, 144 06 E 326 ◦ ◦ ◦ ◦ 41 14 N, 122 23 W 167 332 Table 7.5, 333, 352 Ammersee, Germany 48 N, 11 6 E Caviahue, Lago, Argentina 37◦ 54 S, Great Bear Lake, Canada 66◦ N, 329, 330 Table 7.3 70◦ 35 W 425 120◦ W 323 Aralskoye More, ◦ ◦ ◦ Como, Lago di, Italy 45 58 N, Great Slave Lake, Canada 62 N, Kazakhstan/Uzbekistan 45 N, ◦ ◦ ◦ 9 15 E 330, 331 Table 7.4 114 W 324 60 E 318, 353 ◦ ◦ ◦ Coniston Water, UK 54 20 N, Hamilton Harbour, Lake Ontario, Arresø, Denmark 55 59 N, 12 7 E 3◦ Canada 43◦ ◦ 344 4 W 331, 332 Table 7.5 15 N, 79 51 E 344 Attersee, Austria 47◦ 50 N, 13◦ 35 E Correntoso, Lago, Argentina Hartbeespoort Dam, South Africa 40◦ 24 S, 71◦ 35 W 336 25◦ 24 S, 27◦ 30 E 215 329, 330 Table 7.3 ◦ ◦ ◦ Balaton, Hungary 46◦ 50 N, 18◦42 E Crater Lake, Oregon, USA 42 56 N, Hawes Water, UK 54 31 N, 2 48 W 122◦ 8 W 111, 117 Table 3.2 331, 332 Table 7.5 89, 345, 354 ◦ ◦ ◦ ◦ Crose Mere, UK 52 53 N, 2 50 WE Huron, Lake, Canada/USA 44 30 N, Balkhash, Ozero, Kazakhstan 46 N, ◦ ◦ 109, 117 Table 3.2, 245, 339, 82 W 323 76 E 343, 344 ◦ ◦ ◦ ◦ 368, 373 Iseo, Lago d’, Italy 45 43 N, 10 4 E Bangweolo, Zambia 11 S, 30 E 343 ◦ ◦ Crummock Water, UK 54 31 N, 330, 331 Table 7.4 Bassenthwaite Lake, UK 54 39 N, ◦ ◦ ◦ 3 18 W 332 Table 7.5 Issyk-kul, Ozero, Kyrgyzstan 43 N, 3 12 W 332 Table 7.5 Dead Sea, Israel/Jordan 31◦ 25 N, 78◦ E 89, 325 Bautzen Reservoir, Germany ◦ ◦ ◦ 35 29 W 172 Kaspiyskoye More, Azerbaijan/ 51 11 N, 14 29 E 403 ◦ ◦ ◦ ◦ Derwent Water, UK 54 34 N, 3 8 W Iran/Kazakhstan/Russia/ Baykal, Ozero, Russia 53 N, 108 E 331, 332 Table 7.5 Turkmenistan 42◦ N, 89, 322, 324, 390 Drontermeer, Netherlands 52◦ 16 N, 51◦ E 322 Bayley-Willis, Lago, Argentina ◦ ◦ ◦ ◦ 5 32 E 345 Kasumigaura-Ko, Japan 36 0 N, 40 39 S, 71 43 W 196 ◦ ◦ ◦ ◦ Eglwys Nynydd, UK 51 33 N, 140 26 E 235, 345 Biwa-Ko, Japan 35 N, 136 W 142, 3◦ 44 W 82, 87 Kilotes, Lake, Ethiopia 7◦ 5 N, 219, 327 ◦ ◦ ◦ ◦ 32 N, 25 E 113, 117 Table 3.2 Blelham Tarn, UK 54 24 N, 2 58 W Ennerdale Water, UK 54 38 3◦ 23 W 332 Table 7.5 Kinneret, Yam, Israel 32◦ 50 N, 82, 120, 245, 284, 332 Table 7.5, ◦ ◦ 333 Erie, Lake, Canada/USA 41 45 N, 35 30 E 233, 327, 366 81◦ W 290, 323, 324 Kivu, Lac, D. R. Congo/Rwanda 2◦ S, Bodensee, Austria/Germany/ ◦ ◦ ◦ ◦ ¨ Switzerland 47 40 N, 9 20 E Erken, Sjon, Sweden 59 25 N, 29 E 339, 341 ◦ ¨ ◦ 48 Table 2.2, 71, 329, 330 Table 18 15 E 338 Konigsee, Germany 47 40 N, Espejo, Lago, Argentina 40◦ 36 S, 12◦ 55 E 329, 330 Table 7.3 7.3 ◦ ◦ ◦ 71 48 W 336 Lacar, Lago, Argentina 40 10 S, Brothers Water, UK 54 21 N, ◦ ◦ ◦ Esrum Sø, Denmark 56 00 N, 71 30 W 336 2 56 W 332 Table 7.5 ◦ ◦ ◦ 12 22 E 338 Ladozhskoye, Ozero, Russia 61 N, Budworth Mere, UK 53 17 N, ◦ ◦ ◦ Esthwaite Water, UK 54 21 N, 32 E 89, 324 2 31 W 344 3◦ 0 W 88, 108, 126, 295, 332, Lanao, Philippines 7◦ 52 N, Buenos Aires/General Carrera, Lago, ◦ ◦ ◦ 332 Table 7.5, 370, 371, 390 124 13 E 233, 342, 354 Argentina/Chile 46 35 S, 72 W Eyre, Lake, Australia 29◦ S, 137◦ E Léman, Lac, France/Switzerland 322 ◦ ◦ ◦ ◦ 343 46 22 N, 6 33 E 329, 330 Table Buttermere, UK 54 33 N, 3 16 W Fairmont Lakes Reservoir, 7.3 332 Table 7.5 Minnesota, USA 43◦ 16 N, Llanquihue, Lago, Chile 41◦ 6 S, Cabora Bassa Dam, Mozambique ◦ ◦ ◦ ◦ 93 47 W 416 72 48 W 336 15 38 S, 33 11 E 205 ◦ ◦ ◦ Fonck, Lago, Argentina 41 20 S, Loughrigg Tarn, UK 54 26 N, Carioca, Lagoa, Brasil 19 10 S, ◦ ◦ ◦ 71 44 W 196 3 1 W 332 Table 7.5 42 1 W 115

508 INDEX TO LAKES, RIVERS AND SEAS 509

Lowes Water, UK 54◦ 34 N, 3◦ 21 W Ontario , Lake, Canada/USA Trummen, Sjon,¨ Sweden 56◦ 52 N, 332, 332 Table 7.5 43◦ 40 N, 78◦ W 324 14◦ 50 E 413 Lugano, Lago di, Italy 45◦ 57 N, P. K. le Roux Reservoir, South Africa Turkana (formerly Lake Rudolf), 8◦ 58 E 330, 331 Table 7.4 30◦ 0 S, 24◦ 44 E 113, 117 Kenya/Ethiopia 4◦ N, 36◦ E Maggiore, Lago, Italy/Switzerland Table 3.2 339 46◦ N, 8◦ 40 E 330, 330 Table Ranco, Lago, Chile 40◦ 12 S, Ullswater, UK 54◦ 35 N, 2◦ 53 W 7.3, 331 Table 7.4 72◦ 25 W 336 332, 332 Table 7.5 Malham Tarn, UK 54◦ 6 N, 2◦ 4 W Rapel, Embalse de Chile 34◦ 2 S, Valencia, Lago, Venezuela 10◦ 11 N, 129 71◦ 35 S 233 67◦ 40 W 342 Malaren,¨ Sweden 59◦ 18 N, 17◦ 6 E RedRock Tarn, Australia 38◦ 20 S, Veluwemeer, Netherlands 52◦ 55 N, 198 Fig. 5.6 143◦ 30 W 105 5◦ 45 E 345, 410 Malawi, Lake (formerly Lake Nyasa), Rostherne Mere, UK 53◦ 21 N, Victoria, Lake, Malawi/Mozambique/Tanzania 2◦ 23 W 119, 339, 366 Kenya/Tanzania/Uganda 1◦ S, 12◦ S, 35◦ E 339, 340 Rotongaio, Lake, New Zealand 33◦ E 339, 341 Matano, Danau, Indonesia 2◦ 35 S, 38◦ 40 S, 176◦ 2 E 121 Vierwaldstattersee,¨ Switzerland 121◦ 23 E 322 Rydal Water, UK 54◦ 27 N, 3◦ 0 W 47◦ N, 8◦ 20 E 59, 329, 330 Memphr´emagog, Lac, Canada/USA 332 Table 7.5 Table 7.3 45◦ 5 N, 72◦ 16 W 89 Sagami-Ko, Japan 35◦ 24 N, 139◦ 6 E Villarrica, Lago, Chile 39◦ 15 S, Mendota, Lake, USA 43◦ 21 N, 198 Fig. 5.6 72◦ 35 W 336 89◦ 25 W 289 Schlachtensee, Germany 52◦ 28 N, Volta Grande Reservoir, Brasil Michigan, Lake, USA 43◦ 45 N, 13◦ 25 E 410 20◦ 4 S, 48◦ 13 W 415 86◦ 30 W 290, 323, 324, 390 Schohsee,¨ Germany 54◦ 10 N, Vostok, Lake, Antarctica approx. Mikolajske, Jezioro, Poland 53◦ 10 N, 10◦ 25 E 338 85◦ S, 50◦ W 322 21◦ 33 E 298, 339 Sniardwy,´ Poland 53◦ 45 N, 21◦ 45 E Wahnbach Talsperre, Germany Millstatter¨ See, Austria 46◦ 48 N, 344 50◦ 50 N, 7◦ 8 E 409 13◦ 33 E 325, 350 Søbygaard, Denmark 56◦ 3 N, Walensee, Switzerland 47◦ 7 N, Montezuma’s Well, Arizona, USA 9◦ 40 E 413 9◦ 16 E 330 Table 7.3 34◦ 37 N, 111◦ 51 W 233, 241 St James’s Park Lake, UK 51◦ 30 N, Washington, Lake, Washington, USA Murtensee, Switzerland, 46◦ 55 N, 0◦ 9 E 345 47◦ 35 N, 122◦ 14 W 408 7◦ 5 E 115 Stechlinsee, Germany 53◦ 10 N, Wast Water, UK 54◦ 26 N, 3◦ 17 W Mount Bold Reservoir, Australia, 13◦ 3 E 326, 337 332 Table 7.5 35◦ 0 S, 138◦ 48 E 113, 117 Superior, Lake, Canada/USA Wellington Reservoir, Australia Table 3.2 47◦ 30 N, 89◦ W 117 Table 3.2, 33◦ 20 S, 116◦ 2 EFig29 Nauel Huapi, Lago, Argentina 323 Windermere, UK 54◦ 20 N, 2◦ 53 W 40◦ 50 S, 71◦ 50 W 336 Tahoe, Lake, California/Nevada, USA 80, 115, 117 Table 3.2, 119, 221, Neagh, Lough, UK 54◦ 55 N, 6◦ 30 W 39◦ N, 120◦ W 198 Fig. 5.6 225, 245, 247, 284, 289, 292, 48 Table 2.2, 72, 345 Tai Hu, China 31◦ N, 120◦ E 344 332, 332 Table 7.5, 333, 354, Negra, Laguna, Chile 37◦ 49 S, Tanganyika, Lac, Burundi/ D. R. 368, 401, 402 70◦ 2 W 113 Congo/Tanzania/Zambia 6◦ S, Winnipeg, Lake, Canada 53◦ S, Ness, Loch, UK 57◦ 16 N, 4◦ 30 W 30◦ E 263, 339, 340, 392 98◦ W 343 126, 390 Tchad, Lac, Chad/Niger/Nigeria Wolderwijd, Netherlands 52◦ 29 N, Neusiedlersee, Austria/Hungary 12◦ 30 N, 14◦ 30 E 105, 343, 5◦ 51 E 345 47◦ 47 N, 16◦ 44 E 377 Fig. 7.22 344 Worthersee,¨ Austria 46◦ 37 N, Nyos, Lake, Cameroon 6◦ 40 N, Thames Valley Reservoirs, UK 14◦ 10 E 325 10◦ 13 E 126 51◦ 30 N, 0◦ 40 W 139, 405, 415, Zurichsee,¨ Switzerland 47◦ 12 N, N’zigi (formerly Lake Albert), D. R. 416 8◦ 42 E 59, 235, 330 Table 7.3, Congo/Uganda 1◦ 50 N, 31◦ E Thirlmere, UK 54◦ 32 N, 3◦ 4 W 332 366 339 Table 7.5 Oak Mere, UK 53◦ 13 N, 2◦ 39 W Titicaca, Lago, Bolivia/Peru 15◦ 40 S, 339, 345, 425 69◦ 35 W 342 RIVERS AND Okeechobee, Lake, Florida, USA Todos Los Santos, Lago, Chile ESTUARIES 27◦ N, 81◦ W 413 41◦ 5 S, 72◦ 15 W 336 Onezhskoye, Ozero, Russia 62◦ N, Traful, Lago, Argentina 40◦ 36 S, Angara, Russia 55◦ 50 N, 110◦ 0 E 36◦ E 89, 324, 325 71◦ 25 W 336 322 510 INDEX TO LAKES, RIVERS AND SEAS

Ashes Hollow, UK 52◦ 30 N, 2◦ 50 W Gulf of Bothnia 62◦ N, 20◦ E 112, Trondheimsfjord 64◦ N, 9◦ E 311 48 Table 2.2 312 Ullsfjord 71◦ N, 27◦ E 311 Danube, Romania/Russia 43◦ 15 N, Gulf of Finland 60◦ N, 28◦ E 312 Mediterranean Sea 29◦ 35 E 312 Gulf of Maine 43◦ N, 68◦ W 310, Black Sea 43◦ N, 35◦ E 259, 312 Dnepr, Ukraine 46◦ 30 N, 32◦ 0 E 407 Golfo di Napoli 40◦ 45 N, 14◦ 15 E 313 Gulf of Mexico 25◦ N, 90◦ W 313 Dnestr, Moldova/Ukraine 46◦ 3 N, Gulf Stream (Bahamas) 25◦ N, Tyrrhenian Sea 40◦ N, 12◦ E 30◦ 23 E 312 75◦ W 313 Don, Ukraine 47◦ 11 N, 39◦ 10 E 313 English Channel 50◦ N, 2◦ W 234, Indian Ocean 111, 134, 162 Guadiana, at Mourão, Portugal 310, 311 Andaman Sea 12◦ N, 96◦ E 309 38◦ 24 N, 7◦ 22 W 242 Irish Sea – Clyde Estuary Arabian Sea 15◦ N, 65◦ E 309 Mississippi, USA 29◦ 0 N, 89◦ 20 W 55◦ 50 N, 5◦ 00 W 112 Arafura Sea 10◦ S, 135◦ E 310 126 Irish Sea – Severn Estuary Red Sea 20◦ N, 38◦ E 40 Selenga, Russia 52◦ 15 N, 106◦ 40 E 51◦ 20 N, 4◦ 00 W 48 Table 2.2, Pacific Ocean 322 117 Table 3.2 ALOHA 22◦ 45 N, 158◦ W Severn, UK 51◦ 20 N, 3◦ W 112, 242 Labrador Sea 60◦ N, 55◦ W 306 305 Thames, at Reading, UK 51◦ 27 N, Naragansett Bay (RI) 41◦ 23 N, Baja California 25◦ N, 110◦ W 0◦ 29 W 48 Table 2.2 71◦ 24 W 310 407 White Nile, Sudan/Uganda 15◦ 30 N, NorthAtlantic Drift Current California Current (San Francisco) 32◦ 50 E 339 45◦ N, 45◦ W 289, 306 35◦ N, 115◦ W 309 NorthAtlantic Subtropical Gyre East China Sea 30◦ N, 125◦ E (Mauritania/Senegal) 15◦ N, 310 OCEANS AND SEAS 20◦ W 309 Kuroshio Current 40◦ N, 150◦ E NorthAtlantic Tropical Gyre 5◦ N, 306, 307 Arctic Ocean 15◦ W 306 NorthPacific Subtropical Gyre Polar Basin 80◦ N, 180◦ W 306 North Sea 56◦ N, 4◦ E 1, 310, 407, 25◦ N, 160◦ W 133, 162, 304, Atlantic Ocean 111, 134 427 354, 382 Baltic Sea 55◦ N, 20◦ E 134, 310, Norwegian Sea 70◦ N, 0◦ E 306, Peru Current (Galapagos Islands) 312, 426 307 5◦ S, 90◦ W 134, 309 Bay of Fundy 45◦ N, 66◦ W 42 Øresund 56◦ 00 N, 12◦ 50 E Polar Front ∼40◦ S 308 Benguela Current (Gabon) 0◦ N, Oslofjord 59◦ N, 11◦ E 101, 312 Sea of Okhotsk 55◦ N, 90◦ W 134, 0◦ E 134, 309 Ria de Vigo 42◦ N, 9◦ W 311, 313 310 Canaries Current 30◦ N, 15◦ W 309 Sargasso Sea 30◦ N, 60◦ W 111, 117 South Pacific Gyre 25◦ S, 140◦ W Table 3.2, 162 306 Grand Banks of Newfoundland St Lawrence Estuary 49◦ N, 64◦ W Southern Ocean 60◦ S, 30◦ E 168, 45◦ N, 52◦ W 310, 427 134, 407 306, 307 Index to genera and species of phytoplankton

Generamentionedinthetextarelistedtogetherwiththeirsystematicposition(PhylumORDER)andauthoritiesfor eachspeciesarecited.Synonymsareincludedwhereappropriate.Entriesaresufﬁxed‘M’or‘F’toindicatemarineor freshwateroccurrence,or‘M/F’forgeneraappearinginboth.Theboldentryforfreshwaterspecies(A,B,etc.)refers tothetraitselectedfunctionalgroupingofReynoldsetal.(2002)assummarisedinTable7.1.

Achnanthes(Bacillariophyta AnabaenasolitariaKleb.F,H2233, Aphanizomenonflos-aquaeRalfsex BACILLARIALES)M/F7Table1.1 332,335,336 Born.etFlah.F,H124,26Table AchnanthestaeniataGrun.M306, AnabaenaspiroidesKleb.F,H1338 1.2,184Table5.0,186,219Table 312 Anabaenopsis(Cyanobacteria 5.4, 312, 333, 338, 339, 426 Actinocyclus(Bacillariophyta NOSTOCALES)F6Table1.1,26 Aphanizomenon gracile Lemm. F, BIDDULPHIALES)M/F309,312, Table1.2,81,205,341,344,401 probably H2 233 317,353 Anacystis(Cyanobacteria Aphanocapsa (Cyanobacteria Alexandrium(Dinophyta CHROOCOCCALES)F CHROOCOCCALES) F GONYAULACALES)M233,312, Genusdefunct,partof Several species, all colonial; F, K; 313 Synechococcus free cells are picoplanktic Alexandriumtamarense(Lebour) Anacystisnidulans,seealso Synechoccus, Z BalechM201,311,407 Synechococcus183 Aphanothece (Cyanobacteria Amphidinium(Dinophyta Ankistrodesmus(Chlorophyta CHROOCOCCALES) F, K 6 Table GYMNODINIALES)M7Table1.1 CHLOROCOCCALES)F6Table 1.1, 26 Table 1.2, 320 Table 7.1, Amphisolenia(Dinophyta 1.1,344,425 344 DINOPHYSIALES)M203Table Oncelargegenus,manyseparated Arthrodesmus (Chlorophyta 5.2,234 intoothergenera ZYGNEMATALES) F 6 Table 1.1 Anabaena(Cyanobacteria Ankistrodesmusbraunii184Table Arthrospira (Cyanobacteria NOSTOCALES)mostlyF6Table 5.0 OSCILLATORIALES) mostly F 6 1.1,26Table1.2,58,59,65,67, Ankistrodesmusfalcatus,seealso Table 1.1, 26 Table 1.2, 320 81,121,129,130,165,172,205, Monoraphidiumcontortum338 Table 7.1 206,213,216,226,228,229, Ankyra(Chlorophyta Asterionella (Bacillariophyta 230,232,241,249,271,293, CHLOROCOCCALES)F6Table BACILLARIALES), M/F 7 Table 297,328,329,330,333,340, 1.1,82,212,218,226,228,229, 1.1, 23, 24, 33 Table 1.6, 54, 63, 341,342,344,366,401,404,405 230,231,232,247,274,284, 64, 65, 66, 67, 80, 158, 172, 191, AnabaenacircinalisRabenh.ex 285,300,320Table7.1,333, 192, 195, 196, 197, 201, 202, Born.etFlah.F,H124,26 344,359,370 206, 207, 208, 213, 218, 220, Table1.2,57Table2.4,339 Ankyrajudayi(G.M.Smith)FottF, 221, 222, 224, 225, 226, 228, AnabaenacylindricaLemmermann X120Table1.1,26Table1.2, 231, 233, 242, 245, 246, 248, F,SN?187 219Table5.4,277Table6.3,284 249, 269, 270, 274, 280, 290, Anabaenaflos-aquae(Lyngb.)Bréb. Table6.4,285Table6.5,338 292, 293, 294, 298, 299, 300, exBorn.etFlah.F,H154Table Anthosphaera(Haptophyta 325, 329, 333, 338, 339, 344, 2.3,157Table4.2,165,184 COCCOLITHOPHORIDALES)M 365, 378 Table5.0,194,195,219Table 312 Asterionella formosa Hassall. F, B 5.4,248,320Table7.1,333,338 Apedinella(Chrysophyta and C 20 Table 1.1, 26 Table 1.2, AnabaenalemmermanniiRichterF, PEDINELLALES)M7Table1.1 29 Table 1.3, 31, 31 Table 1.5, H258,233,312,320Table7.1, Apedinellaspinifera(Throndsen) 32, 52, 54 Table 2.3, 61 Table 322,332,426 ThrondsenM35Table1.7 2.5, 63, 66, 107, 113, 119, 129, AnabaenaminutissimaPridmoreF, Aphanizomenon(Cyanobacteria 157 Table 4.2, 184 Table 5.1, SN320Table7.1 NOSTOCALES)mostlyF6Table 195, 197, 202, 219 Table 5.4, AnabaenaovalisporumFortiF,H2 1.1,26Table1.2,59,67,81,129, 220, 221 Table 5.5, 221 Table 327 165,205,216,230,233,320 5.6, 232, 245, 246, 247, 277 AnabaenaplanctonicaBrunnth.F, Table7.1,325,330,341,401, Table 6.3, 320 Table 7.1, 324, H2?338 404,405 326, 328, 330, 331, 338

511 512 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON

Asterionella(Bacillariophyta)(cont.) Calciopappus(Haptophyta Chaetocerosdiadema(Ehrenb.)Gran AsterionellajaponicaCleveM234, COCCOLITHOPHORIDALES)M M306,310 311 312 ChaetocerosneglectusKarstenM308 Aulacoseira(Bacillariophyta Carteria(ChlorophytaVOLVOCALES) ChaetocerosradicansSchut¨ tM311 BIDDULPHIALES)F7Table1.1, F234,311 ChaetocerossocialisLauderM311, 23,28,54,62,63,130,177,213, Cerataulina(Bacillariophyta 312,313 214,243,245,249,250,325, BIDDULPHIALES)M7Table1.1, Chilomonas(Cryptophyta 329,336,341,342,344,415 234,312,317 CRYPTOMONADALES)F6Table Aulacoseiraalpigena CerataulinabergoniiH.Perag.M 1.1 (Grun.)KrammerF,A(also 312 Chlamydocapsa(Chlorophyta recordedasMelosiradistans)203 Cerataulinapelagica(Cleve)Hendey TETRASPORALES)F293 Table5.2 M311,312 Chlamydocapsaplanctonica(W.and Aulacoseiraambigua(Grun.) Ceratium(Dinophyta .G.S.West)FottF,F(formerly Simonsen232,320Table7.1, GONYAULACALES,M/F7Table knownasGloeocystisplanctonica) 326 1.1,13,24,60,68,88,206,213, 57Table2.4 Aulacoseirabaicalensis(K.I.Mey.) 216,218,219,228,230,231, Chlamydomonas(Chlorophyta SimonsenF,A322 232,233,234,249,293,295, VOLVOCALES)M/F6Table1.1, AulacoseirabinderanaKutz¨ .F,B26 311,320Table7.1,329,330, 35Table1.7,49,78,212, Table1.2 331,332,333,338,339,348, 232,233,312,326,333,343,352,425 Aulacoseiragranulata(Ehrenb.) 366,370,371,381,385 ChlamydomonasreinhardtiiP.A. SimonsenF,P6Table1.1,29 Ceratiumarcticum(Ehrenb.)Cleve DangeardF,X1127,157Table Table1.3,123,219Table5.4, M306,307 4.2 232,320Table7.1,324,327, CeratiumazoricumCleveM307 Chlorella(Chlorophyta 328,330,336,339,340,341, CeratiumcarrienseGourretM307 CHLOROCOCCALES)F32,33 373 Ceratiumfurca(Ehrenb.)M307, Table1.6,113,127,137,148, Aulacoseiraislandica(O.Muller)¨ 310,311,316 150,182,184Table5.0,188, SimonsenF,C225,233,320 Ceratiumfusus(Ehrenb.)M234, 196, 207, 208, 209, 212, 230, Table7.1,322,323,324,330 306,307,310,311,312,313, 231, 260, 298, 320 Table 7.1, Aulacoseirasolida(Eulenstein) 316 324, 333, 343, 344, 352, 357, KrammerF,B225,233,320 CeratiumhexacanthumGourretM 365, 370, 378, 425 Table7.1,322,323,324,330 307 Chlorella minutissima Fott et Aulacoseirasubarctica(O.Muller)¨ Ceratiumhirundinella(O.F.Muller)¨ Novakov´ aF,´ X3 203 Table 5.2, HaworthF,B29Table1.3,54 DujardinF,LM6Table1.1,20 332 Table2.3,61Table2.5,62,129, Table1.1,83,129,184Table5.0, Chlorella pyrenoidosa Chick F X1 20 202,225,233,247,320Table 205,216,219Table5.4,229, Table 1.1, 26 Table 1.2, 157 7.1,324,325,331,333 248,325,338,339 Table 4.2, 424 Aureococcus(Bacillariophyta Ceratiumlineatum(Ehrenb.)M307 Chlorella vulgaris Beijerinck F, X1 BIDDULPHIALES)M407 Ceratiumlongipes(Bail.)GranM (includes strains formerly 306,307,310,312 known as Chlorella pyrenoidosa) Bacillaria(Bacillariophyta Ceratiumtripos(O.F.Muller)¨ 54 Table 2.3, 61 Table 2.5 BIDDULPHIALES)M NitzschM305,307,310,311, Chlorobium (Anoxyphotobacteria)F Bacteriastrum(Bacillariophyta 312,313,316 321 Table 7.1 BIDDULPHIALES)M203Table Chaetoceros(Bacillariophyta Chlorobotrys (Eustigmatophyta)F6 5.2,311 BIDDULPHIALES)mostlyM7 Table 1.1, 424 Binuclearia(Chlorophyta Table1.1,60,306,307,310,311, Chlorococcum (Chlorophyta ULOTRICHALES)F233,259 312,313,314,317,353 CHLOROCOCCALES) F 54 Table Bitrichia(Chrysophyta ChaetocerosatlanticumCleveM308 2.3, 61 Table 2.5, 352 HIBBERDIALES)F7Table1.1 ChaetoceroscompressusLauderM Chlorogonium (Chlorophyta Botryococcus(Chlorophyta 234,310,311,312 VOLVOCALES) F 326 CHLOROCOCCALES)F6Table ChaetocerosconvolutumCastracene Choricystis (Chlorophyta 1.1,54,320Table7.1,322,339, M307 CHLOROCOCCALES) F 6 Table 344 ChaetoceroscurvisetumCleveM313 1.1, 328 BotryococcusbrauniiKutzin¨ gF,F ChaetocerosdebilisCleveM309, Chromatium (Anoxyphotobacteria)F 331,425 310,311,312 321 Table 7.1 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON 513

Chromulina(Chrysophyta Coelastrum(Chlorophyta CryptomonaserosaEhrenb.F,Y334 CHROMULINALES)F7Table1.1, CHLOROCOCCALES)F320Table CryptomonasmarssoniSkujaF,Y 20Table1.1,247,251,284,300, 7.1,341,344 334 328,425 CoelastrummicroporumNa¨ geliF,J CryptomonasovataEhrenb.F,Y6 Chroococcus(Cyanobacteria Coenochloris(Chlorophyta Table1.1,20Table1.2,184 CHROOCOCCALES)F6Table CHLOROCOCCALES)F24, Table5.0,219Table5.4,226, 1.1,26Table1.2,171,325,327 56,82,129,203Table5.2, 276, 277 Table 6.3, 334, 338, Chroomonas(Cryptophyta 210,228,273,293,320 339 CRYPTOMONADALES)M/F6 Table7.1,325,326,340, Cryptomonas profunda Butcher M Table1.1,338 359 35 Table 1.7 Chroomonassalina(Wislouch) Coenochlorisfottii(Hindak)´ Cyanobium (Cyanobacteria ButcherM35Table1.7 TsarenkoF,F(formerlyknown CHROOCOCCALES), F 213, 269, Chrysochromulina(Haptophyta asSphaerocystisschroeteri)57 327 PRYMNESIALES)M/F7Table1.1, Table2.4,219Table5.4,230, Picoplanktic Z,free cells of 13,233,234,251,312,320Table 248,331 Cyanodictyon or Synechocystis 7.1,323,324,327,330,331,336, Coenococcus(Chlorophyta Cyanodictyon (Cyanobacteria 338,343,402 CHLOROCOCCALES)F231 CHROOCOCCALES) F 213, 269 Chrysochromulinaherdlensis Coenocystis(Chlorophyta Two species, all colonial; F, K?; LeadbeaterM35Table1.7 CHLOROCOCCALES)F203Table free cells are picoplanktic ChrysochromulinaparvaLackeyF, 5.2,212 Cyanobium, Z X220Table1.1,338 Genusincludessomespecies Cyanophora (Glaucophyta)F,X1 6 ChrysochromulinapolylepisManton previouslyattributedto Table 1.1, 11 etParkeM312,407 Coccomyxa Cyanothece (Cyanobacteria Chrysococcus(Chrysophyta Corethron(Bacillariophyta CHROOCOCCALES), F 269 CHROMULINALES)F7Table1.1, BIDDULPHIALES)M307,311 Relatively new genus 20Table1.1,251,320Table7.1, CorethroncriophilumCastraceneM accommodating larger species 332 306,308 of Synechococcus, X2? Chrysolykos(Chrysophyta CorethronhystrixHensenM307 Cyathomonas (Cryptophyta CHROMULINALES)F7Table1.1, Coscinodiscus(Bacillariophyta CRYPTOMONADALES) M/F 159, 203Table5.2 BIDDULPHIALES)mostlyM307, 425 Chrysosphaerella(Chrysophyta 309,310,312,317,341 Cyclococcolithus (Haptophyta CHROMULINALES)F7Table1.1, CoscinodiscussubbulliensJørgensen COCCOLITHOPHORIDALES) M 129,213 M306 234 Clathrocystis(Anoxyphotobacteria)F CoscinodiscuswailseiiGranetAngst. Cyclococcolithus fragilis (Lohmann) 6Table1.1 M50,53 Deﬂandre M 234 Closterium(Chlorophyta Cosmarium(Chlorophyta Cyclostephanos (Bacillariophyta ZYGNEMATALES)F6Table1.1, ZYGNEMATALES)F6Table1.1, BIDDULPHIALES) F 340, 341 23,192,340,341,344 129,202,203Table5.2,233, Cyclotella (Bacillariophyta ClosteriumaciculareT.West 279,320Table7.1,331,336, BIDDULPHIALES) M/F 7 Table F,P20Table1.1,26 385,424 1.1, 23, 63, 129, 195, 197, 201, Table1.2,219Table5.4, CosmariumabbreviatumRaciborski 202, 208, 225, 232, 249, 313, 232,320Table7.1,328, F,N195,201,247,332 325, 326, 353 330,339 CosmariumcontractumKirchnerF, Cyclotella bodanica Eulenstein F, A ClosteriumacutumBréb.F,P15Fig N332 323, 329, 385 1.1 Cosmariumdepressum(Na¨ geli) Cyclotella caspia Grun. M 234, 312, Coccolithus(Haptophyta LundellF,N20Table1.1 313, 317 COCCOLITHOPHORIDALES)M7 Crucigena(Chlorophyta Cyclotella comensis Grunow F, A 203 Table1.1 CHLOROCOCCALES)F231 Table 5.2, 320 Table 7.1, 325, Coccolithuspelagicus(Wallich) Cryptomonas(Cryptophyta 331 SchillerM35Table1.7 CRYPTOMONADALES)M/F6 Cyclotella glomerata Bachm. F, A Coccomyxa(Chlorophyta Table1.1,228,229,230,247, 203 Table 5.2, 323, 325, CHLOROCOCCALES)F352 260,269,274,284,300,312,320 329 Someplankticspeciesarenowin Table7.1,323,324,328,330, Cyclotella litoralis Lange et Coenocystis 335,338,359 Syvertsen M 309, 317 514 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON

Cyclotella(cont.) DinobryonsertulariaEhrenb.F,E EuglenamutabilisF.SchmitzF,W1 CyclotellameneghinianaKutz¨ .F,B 331 424,425 20Table1.1,61Table2.5,195, DinobryonsocialeEhrenb.F,E157 Eunotia(Bacillariophyta 197 Table4.2 BACILLARIALES)M/F425 CyclotellananaHustedtM53 Dinophysis(Dinophyta Eutetramorus(Chlorophyta CyclotellapraeterissimaLundF,B20 DINOPHYSIDALES)M203Table CHLOROCOCCALES)F Table1.1,202,247,331 5.2,309,311,313 Redundantgenusname–see Cyclotellaradiosa(Grun.) DinophysisacuminataClap.etLach. Coenococcus LemmermannF,A(formerly M310 Eutreptia(Euglenophyta knownasCyclotellacomta)203 Ditylum(Bacillariophyta EUTREPTIALES)M6Table1.1, Table5.2,233,323,326,331 BIDDULPHIALES)M55,130 234,311,312 Cylindrocystis(Chlorophyta Ditylumbrightwellii(West)Grun.M Eutreptiella(Euglenophyta ZYGNEMATALES)F424 55,130 EUTREPTIALES)M313 Cylindrospermopsis(Cyanobacteria Dunaliella(Chlorophyta Exuviella(Dinophyta NOSTOCALES)F,SN6Table1.1, VOLVOCALES)M6Table1.1,32, PROROCENTRALES)M7Table 26Table1.2,205,320Table7.1, 78,234,311 1.1,307,353 340,341,342,344,366,401 DunaliellatertiolectaButcherM35 ExuviellabalticaLohm.M312 Cylindrospermopsisraciborskii Table1.7 Florisphaera(Haptophyta (Woloszynska)Seenayyaet COCCOLITHOPHORIDALES)M7 SubbaRajuF,SN216,384 Elakatothrix(Chlorophyta Table1.1,309 ULOTRICHALES)F6Table1.1 Fragilaria(Bacillariophyta Dactylococcopsis(Cyanobacteria Emiliana(Haptophyta BACILLARIALES)M/F7Table1.1, CHROOCOCCALES),F325 COCCOLITHOPHORIDALES)M7 24,51,63,226,228,229,232, Detonula(Bacillariophyta Table1.1,13,203Table5.2,311, 233,245,249,269,300,330, BIDDULPHIALES)M7Table1.1 312 338 Detonulapumila(Castracene)Gran Emilianahuxleyi(Lohm.)Hayet FragilariacapucinaDesmaz.F,P6 M35Table1.7 Mohl.M35Table1.7,130,234, Table1.1 Diacanthos(Chlorophyta 307,310,313 FragilariacrotonensisKittonF,P6 CHLOROCOCCALES)F,X3352 Ethmodiscus(Bacillariophyta Table1.1,20Table1.1,23,29 Diacronema(Haptophyta BIDDULPHIALES)M50,234 Table1.3,31Table1.5,54Table PAVLOVALES)M7Table1.1 Ethmodiscusrex(Rattray)Wiseman 2.3,57Table2.4,61Table2.5, Diatoma(Bacillariophyta etHendeyM50,234 62,63,66,129,184Table5.0, BACILLARIALES)F7Table1.1, Euastrum(Chlorophyta 219 Table 5.4, 232, 247, 320 324 ZYGNEMATALES)F6Table1.1 Table 7.1, 324, 333, 336, 339 Diatomaelongatum(Lyngb.)C. Eucampia(Bacillariophyta Fragilaria oceanica Cleve M 307, AgardhF,C172,338 BIDDULPHIALES)M311,312 311 Dictyosphaerium(Chlorophyta Eucampiacornuta(Cleve)Grun.M Fragilariopsis (Bacillariophyta CHLOROCOCCALES)F6Table 311 BACILLARIALES) M 7 Table 1.1, 1.1,210,336 EucampiazodiacusEhrenb.M 307, 308 Dictyosphaeriumpulchellum 312 Fragilariopsis cylindrus (Grun.) H.C.WoodF,F20Table1.1,331 Eudorina(ChlorophytaVOLVOCALES) Krieger M 311 Dinobryon(Chrysophyta F6Table1.1,24,182,211,216, Fragilariopsis doliolus Wallich M CHROMULINALES)F7Table1.1, 228,229,230,232,247,269, 309 89,129,130,210,219Table5.4, 270,293,299,320Table7.1, Fragilariopsis nana (Steemann 228,229,231,232,320Table 338,343 Nielsen) Paasche M 307 7.1,323,325,329,330,333,334, EudorinaelegansEhrenb.F,G?26 336,338,385 Table1.2,157Table4.2 Geminella (Chlorophyta DinobryonbavaricumImhofF,E EudorinaunicoccaG.M.SmithF,G ULOTRICHALES) F, T 6 Table 1.1, 331 26Table1.2,57Table2.4,184 233, 294, 320 Table 7.1 DinobryoncylindricumImhofF,E Table5.0,219Table5.4,226, Gephyrocapsa (Haptophyta 203Table5.2,322,326,331 339 COCCOLITHOPHORIDALES) M 7 DinobryondivergensImhofF,E20 Euglena(Euglenophyta Table 1.1, 203 Table 5.2 Table1.1,184Table5.0,331, EUGLENALES)M/F6Table1.1, Gephyrocapsa oceanica Kamptner M 336,338 343,425 234 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON 515

Glaucocystis (Glaucophyta)F6 Gyrodinium uncatenatum Hulbert M Kirchneriella (Chlorophyta Table 1.1 35 Table 1.6 CHLOROCOCCALES) F 6 Table Glenodinium (Dinophyta Gyrosigma (Bacillariophyta 1.1, 336 PERIDINIALES) F 7 Table 1.1, 13, BACILLARIALES) F, D 344 Koliella (Chlorophyta 324, 334 ULOTRICHALES) F 6 Table 1.1, Gloeocapsa (Cyanobacteria Halosphaera (Prasinophyta, 320 Table 7.1 CHROOCOCCALES) F 325 HALOSPHAERALES) M 306 Koliella longiseta (Vischer) Hindak´ Gloeotrichia (Cyanobacteria Hemiaulus (Bacillariophyta F, X3 332 NOSTOCALES) F 6 Table 1.1, 26 BIDDULPHIALES) M 166, 305, Table 1.2, 67, 81, 129, 205, 213, 385 Lagerheimia (Chlorophyta 216, 338, 401 Hemiaulus hauckii Grun. M 311, CHLOROCOCCALES) F Gloeotrichia echinulata (J. E. Smith) 316, 317 344 Richter F, H2 216, 320 Table 7.1, Hemidinium (Dinophyta Lagerheimia genevensis (Chodat) 338 PHYTODINIALES) F 7 Table 1.1 Chodat F, X1 425 Golenkinia (Chlorophyta Hemiselmis (Cryptophyta Lauderia (Bacillariophyta CHLOROCOCCALES) F, X1 320 CRYPTOMONADALES) M 234 BIDDULPHIALES) M Table 7.1, 352 Heterocapsa (Dinophyta Lauderia annulata Cleve M Gomphosphaeria (Cyanobacteria PERIDINIALES) M 233, 234, 311 CHROOCOCCALES) F 6 Table 312 Lauderia borealis Gran M 312 1.1, 26 Table 1.2, 81, 166, 205, Heterocapsa triquetra (Ehrenb.) Lepocinclis (Euglenophyta 233, 330, 332, 338 Stein M 310, 311, 312, 313, 316 EUGLENALES) F, W1 6 Table 1.1, Main species G. naegeliana Heterosigma (Raphidophyta 343, 425 transferred to Woronichinia CHLOROMONADALES) M Leptocylindrus (Bacillariophyta Goniochloris (Xanthophyta Heterosigma carterae (Hulbert) BIDDULPHIALES) M 203 Table MISCHOCOCCALES) F 6 Table Taylor M 35 Table 1.6 5.2, 312, 317 1.1 Histoneis (Dinophyta DINOPHYSALES) Leptocylindrus danicus Cleve M 309, Gonium (Chlorophyta VOLVOCALES) M 203 Table 5.2 310, 311 F, W1 321 Table 7.1, 343 Limnothrix (Cyanobacteria Gonyostomum (Raphidophyta Isochrysis (Haptophyta OSCILLATORIALES) F 6 Table CHLOROMONADALES) F 6 PRYMNESIALES) M 7 Table 1.1, 1.1, 26 Table 1.2, 114, 191, 213, Table 1.1, 12, 321 Table 7.1 234 401, 405 Gonyostomum semen (Ehrenb.) Isochrysis galbana Parke M 35 Limnothrix redekei (van Goor) Diesing F, Q 344 Table 1.7 Meffert F, S1 206, 233, 320 Gymnodinium (Dinophyta Table 7.1, 345, 366, 416 GYMNODINIALES) M/F 7 Table Karenia (Dinophyta Lingulodinium (Dinophyta 1.1, 233, 311, 325, 326, 328, 336, GYMNODINIALES) M 233 GONIAULACALES) M 7 Table 1.1, 425 Karenia brevis (Davis) G. Hansen et 68, 311 Gymnodinium baicalense Authority Moestrup M 408 Lingulodinium polyedrum (Stein) not found F 322 Karenia mikimotoi (Miyake et Dodge M 234, 309, 316, 408 Gymnodinium catenatum Graham M Kominami) G. Hansen et Lyngbya (Cyanobacteria 68, 233, 309, 408 Moestrup M 35 Table 1.6, 310, OSCILLATORIALES) F 6 Table Gymnodinium helveticum Penard F 311, 312, 316, 408 1.1, 26 Table 1.2, 59, 325 131, 324 Katablepharis (Cryptophyta Lyngbya limnetica Lemm. F, R Gymnodinium sanguineum Hirasaka CRYPTOMONADALES) M 159 211 M 35 Table 1.6 Katodinium (Dinophyta Gymnodinium simplex Lohm. M 35 GYMNODINIALES) M/F 316 Mallomonas (Chrysophyta Table 1.6 Kephyrion (Chrysophyta SYNURALES) F 7 Table 1.1, 23, Gymnodinium uberrimum (Allman) CHROMULINALES) F 7 Table 1.1 129, 232, 293, 320 Table 7.1, Kofoid et Swezey F 324 Kephyrion littorale Lund F, X1 20 323 Gymnodinium vitiligo Ballantine M Table 1.1 Mallomonas akrokomos Ruttner in 35 Table 1.6 Keratococcus (Chlorophyta Pascher F, X1 333 Gyrodinium (Dinophyta CHLOROCOCCALES) F Mallomonas caudata Iwanoff F, X2 PERIDINIALES) M 7 Table 1.1, Keratococcus raphidioides Hansgirg 20 Table 1.1, 130, 203 Table 5.2, 233, 234, 316 F, X1 425 331 516 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON

Mantoniella(Prasinophyta Monoraphidium griffithii (Berkeley) Many planktic genera reclassiﬁed CHLORODENDRALES)M6Table Komarkov´ a-Legnerov´ aF,´ X1 into Limnothrix, Planktothrix and 1.1 (taxon rationalises various Tychonema MantoniellasquamataMantonet species and subspecies of ParkeM35Table1.7 Ankistrodesmus) Pandorina (Chlorophyta Melosira(Bacillariophyta Mougeotia (Chlorophyta VOLVOCALES) F 6 Table 1.1, 232, BIDDULPHIALES)F344 ZYGNEMATALES) F, T 233, 320 338, 343 MelosiravariansAgardhF,D344 Table 7.1, 330, 336 Pandorina morum (O. F. Muller)¨ Merismopedia(Cyanobacteria Nannochloris (Chlorophyta Bory F, G 219 Table 5.4, 329 CHROOCOCCALES)F,LO6 VOLVOCALES) M 6 Table 1.1, Paulschulzia (Chlorophyta Table1.1,26Table1.2,165,171, 234, 311, 425 TETRASPORALES) F 6 Table 1.1, 325,326 Nannochloris ocelata Droop M 35 129 Micractinium(Chlorophyta Table 1.7 Paulschulzia pseudovolvox (Schulz) CHLOROCOCCALES)F,X1352 Nephrodiella (Xanthophyta Skuja F, F 331 Microcystis(Cyanobacteria MISCHOCOCCALES) F 6 Table Pavlova (Haptophyta PAVLOVALES) M CHROOCOCCALES)6Table1.1, 1.1 7 Table 1.1, 234 24,26Table1.2,50,55,59,67, Nephroselmis (Prasinophyta Pavlova lutheri (Droop) Green M 81,82,87,113,123,129,165, CHLORODENDRALES) M/F 6 (formerly known as Monochrysis 166,179,184,186,190,192,205, Table 1.1 lutheri) 32, 35 Table 1.7 206,208,213,214,215,226, Nitzschia (Bacillariophyta Pediastrum (Chlorophyta 228,229,231,232,247,249, BACILLARIALES) M/F 7 Table 1.1, CHLOROCOCCALES) F 6 Table 267,269,271,272,275,279, 194, 234, 307, 308, 313, 340, 1.1, 51, 192, 211, 320 Table 7.1, 285,292,293,297,298,299, 424 324, 339, 341, 344 300,320Table7.1,327,328, Nitzschia acicularis (Kutz.)¨ W. Smith Pediastrum boryanum (Turpin) 339,341,344,348,353,359, F 320 Table 7.1, 322, 342 Meneghin F, J 20 Table 1.1 366,370,381,401,403,404,405 Nitzschia bicapitata Lagerstedt M Pediastrum duplex Meyen F, J 67 Microcystisaeruginosa(Kutz.)¨ 309 Pedinella (Chrysophyta emend.ElenkinF,LM,M26 Nitzschia closterium W. Smith M PEDINELLALES) F 7 Table 1.1 Table1.2,54Table2.3,57Table 308 Pedinomonas (Prasinophyta 2.4,58,81,129,157Table4.2, Nodularia (Cyanobacteria PEDINOMONADALES) F 6 Table 184Table5.0,198,209,219,219 NOSTOCALES) M/F 6 Table 1.1, 1.1 Table 5.4, 333, 339, 345 26 Table 1.2, 165, 205 Pelagococcus (Chrysophyta Microcystis wesenbergii (Komarek)´ Nodularia spumigenea Mertens ex PEDINELLALES) M 7 Table 1.1, Komarek´ in Kondrat’eva 195, Born et Flah. M/F H1 312, 426 35 Table 1.7 219, 271 Pelagomonas (Chrsophyta Micromonas (Prasinophyta Ochromonas (Chrysophyta PEDINELLALES) M 7 Table 1.1, CHLORODENDRALES) M 6 Table CHROMULINALES) F, X3 7 Table 305, 308 1.1, 234, 312 1.1, 131, 159, 251, 312, 323, 328, Pelodictyon (Anoxyphotobacteria)F6 Micromonas pusilla (Butcher) 330, 331, 425 Table 1.1 Manton et Parke M 35 Table 1.7 Oocystis (Chlorophyta Peridinium (Dinophyta Monochrysis (Chrysophyta CHLOROCOCCALES) F 6 Table PERIDINIALES) M/F 7 Table 1.1, CHROMULINALES) M, F 332 1.1, 104, 233, 312, 324, 325, 326, 13, 68, 157 Table 4.2, 165, 213, Monodus (Eustigmatophyta)F6 340 233, 307, 311, 326, 327, 342, Table 1.1, 20 Table 1.1 Oocystis lacustris Chodat F, F 129, 366, 385 Monodus subterraneus 184 Table 5.0 203 Table 5.2, 231, 320 Peridinium aciculiferum Monoraphidium (Chlorophyta Table 7.1 Lemmermann F, W2 326 CHLOROCOCCALES) F 6 Table Ophiocytium (Xanthophyta Peridinium bipes Stein F, LM? 1.1, 23, 312, 320 Table 7.1, 324, MISCHOCOCCALES) F 6 Table 336 333, 338, 343, 344, 352 1.1 Peridinium cinctum (O. F. Muller)¨ Monoraphidium contortum (Thuret) Ornithocercus (Dinophyta Ehrenb. F, LM 20 Table 1.1, 219 Komarkov´ a-Legnerov´ aF,´ X1 DINOPHYSIALES) M 203 Table Table 5.4, 338 (taxon rationalises various 5.2, 234, 306, 314, 316 Peridinium depressum Bail. M 306, species and subspecies of Oscillatoria (Cyanobacteria 307 Ankistrodesmus) 26 Table 1.2 OSCILLATORIALES) F 115 Peridinium faroense Paulsen M 310 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON 517

PeridiniumgatunenseNygaardF,LO 191,207,208,209,213,225, Prorocentrum minimum (Pavillard) 205,218,327 228,241,259,269,271,275, Schiller M 312 Peridiniuminconspicuum 350,358,365,370,381,401, Protoperidinium (Dinophyta LemmermannF,LO332,336, 405 PROROCENTRALES) M 313 338 Planktothrixagardhii(Gom.)Anagn. Prymnesium (Haptophyta PeridiniumlomnickiiWooszyskaF,Y etKom.F,S1(formerlyknown PRYMNESIALES) M 7 Table 1.1, 320Table7.1,334 asOscillatoriaagardhii)54Table 35 Table 1.7, 251, 270, 353, 402, PeridiniumovatumPouchetM306 2.3,115,157Table4.2,184 407 PeridiniumpallidumOstenfeldM Table5.0,186,190,191,192, Prymnesium parvum N. Carter M 306 193, 206, 207, 231, 233, 320 313, 316 PeridiniumumbonatumSteinF,LO Table 7.1, 324, 325, 333, 339, Pseudanabaena (Cyanobacteria 232,338,425 345, 366, 378, 408, 410, 416, OSCILLATORIALES) F 6 Table PeridiniumvolziiLemmermannF, 422 1.1, 26 Table 1.2, 233, 320 Table LO336 Planktothrix mougeotii (Bory ex 7.1, 345 PeridiniumwilleiHuitfeldt-KaasF, Gom.) Anagn. et Kom. F, R Pseudanabaena limnetica (Lemm.) LO232,320Table7.1,325,331, (formerly known as Oscillatoria Komarek´ F, S1 416 332,336 agardhii var. isothrix) 26 Table Pseudonitzschia (Bacillariophyta Phacotus(ChlorophytaVOLVOCALES) 1.2, 33, 59, 219 Table 5.4, 226, BACILLARIALES) M 307, 311, 312 F6Table1.1,172,343 233, 320 Table 7.1, 332 Pseudonitzschia delicatissima (P. T. Phacus(EuglenophytaEUGLENALES) Planktothrix prolifica (Gom.) Anagn. Cleve) M (formerly known as F6Table1.1,343 et Kom. F, R (formerly known Nitzschia delicatissima) 307, 311, Phacuslongicauda(Ehrenb.) as Oscillatoria prolifica) 59, 312 DujardinF,W115Fig1.2 193 Pseudopedinella (Chrysophyta Phaeocystis(Haptophyta, Planktothrix rubescens (Gom.) PEDINELLALES) M/F 7 Table 1.1, PRYMNESIALES)M7Table1.1, Anagn. et Kom. F, R (formerly 312, 332 13,24,234,271,306,308,311, known as Oscillatoria rubescens) Pseudopedinella pyriformis N. Carter 385,407 59, 115, 193, 211, 233, 234, 320 M 35 Table 1.7 PhaeocystisantarcticaKarstenM Table 7.1, 325, 328, 330, 346, Pseudosphaerocystis (Chlorophyta 308 366, 409 TETRASPORALES) F 6 Table 1.1, Phaeocystispouchetii(Hariot) Platymonas (Prasinophyta 56, 129, 211, 293, 320 Table 7.1, LagerheimM35Table1.7,312 CHLORODENDRALES) M 311 324 Phaeodactylum(Bacillariophyta Plectonema (Cyanobacteria Pseudosphaerocystis lacustris BACILLARIALES)177 OSCILLATORIALES) F 166 (Lemm.) Novak´ F, F PhaeodactylumtricornutumBohlin Porosira (Bacillariophyta (formerly known as Gemellicystis M28 BIDDULPHIALES) M 310, 311 neglecta) 57 Table 2.4, 231, 248, Plagioselmis(Cryptophyta Porosira glacialis (Grun.) Jørgensen 331 CRYPTOMONADALES)F6Table M 310, 311 Pyramimonas (Prasinophyta 1.1,218,225,230,232,233,284, Prochlorococcus (Cyanobacteria PYRAMIMONADALES) M 308, 320Table7.1,323,324,327, PROCHLORALES) M 6 Table 1.1, 313 330,331,336,338,343,425 11, 26 Table 1.2, 203 Table 5.2, Pyrenomonas (Cryptophyta, Plagioselmisnannoplanctica(Skuja) 213, 305, 306, 316, 322 CRYPTOMONADALES) M 6 Novarinoetal.F,X2(formerly Prochloron (Cyanobacteria Table 1.1 knownasRhodomonasminuta) PROCHLORALES) M 6 Table 1.1, Pyrenomonas salina (Wislouch) 20Table1.1,172,219Table5.4, 11, 26 Table 1.2 Santore M 277Table6.3,338 Prochlorothrix (Cyanobacteria Pyrocystis (Dinophyta Planktolyngbya(Cyanobacteria PROCHLORALES) F, T? 6 Table GONIAULACALES) M 13, 234, OSCILLATORIALES)F59,115, 1.1, 11, 26 Table 1.2 305, 316 342 Prorocentrum (Dinophyta Pyrocystis noctiluca Murray M Planktolyngbyalimnetica(Lemm.) PROROCENTRALES) M 7 Table 55 Komar´ kova-Legner´ ova´ et 1.1, 233, 234, 305, 311, 313 Pyrodinium (Dinophyta CronbergF,R193 Prorocentrum balticum (Lohm.) GONIAULACALES) M 316, 408 Planktothrix(Cyanobacteria Loeblich M 311 Pyrodinium bahamense (Bohm)¨ OSCILLATORIALES)F6Table Prorocentrum micans Ehrenb. M Steidinger et al. M 316, 1.1,23,26Table1.2,58,83,114, 312, 313 408 518 INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON

Radiococcus(Chlorophyta Scrippsiellatrochoidea(Stein) Staurodesmustriangularis CHLOROCOCCALES)F LoeblichM310,311,312,313, (Lagerheim)TeilingF,N336 RadiococcusplanctonicusLundF,F 316 Stephanodiscus(Bacillariophyta (formerlyknownasCoenococcus Skeletonema(Bacillariophyta BIDDULPIALES)F7Table1.1, planctonicus)248,331 BIDDULPIALES)M7Table1.1, 23,53,54,63,148,214,233, Rhizosolenia(Bacillariophyta 312,317 243,245,249,279,329,344 BIDDULPIALES)M7Table1.1, SkeletonemacostatumGrev.M33, Stephanodiscusbinderanus(Kutz.¨ )W. 203Table5.2,234,305,306, 130,234,306,309,311,312,313 Krieg.F,B(formerlyknownas 307,313 Snowella(Cyanobacteria Melosirabinderana)198,322, RhizosoleniaalataBrightw.M130, CHROOCOCCALES)F6Table 324 307,308,310,311,312 1.1,24,26Table1.2 StephanodiscushantzschiiGrun.F,D Rhizosoleniacalcar-avisSchultzeM Sphaerella(Chlorophyta 6Table1.1,20Table1.1,29 311,313,316,317 VOLVOCALES)F Table1.3,31Table1.5,184 RhizosoleniadelicatulaCleveM309, (Mostspeciestransferredto Table5.0,320Table7.1,338 310,311,312 Haematococcus)425 StephanodiscusminutulusCleveet RhizosoleniafragilissimaBergonM Sphaerocauum(Cyanobacteria MollerF,B(formerlyknownas 312 CHROOCOCCALES)F,M320 S.astraeavar.minutula)333, RhizosoleniahebetataBail.M306, Table7.1 338 307,308,310 Sphaerocystis(Chlorophyta Stephanodiscusrotula(Kutz.)¨ RhizosoleniasetigeraBrightw.M60 CHLOROCOCCALES)F HendeyF,C(formerlyknownas RhizosoleniastolterforthiiH.Perag. (someformerspeciesnowin S.astraea)6Table1.1,20Table M309 Coenochloris)82,203Table5.2 1.1,29Table1.3,31Table1.5, RhizosoleniastyliformisBrightw.M SphaerocystisschroeteriChodatF,F 50,52,54Table2.3,61Table 305,306,307,310,311,316,317 194 2.5,66,232,320Table7.1,338, Rhodomonas(Cryptophyta, Spirulina(Cyanobacteria 339 CRYPTOMONADALES)M/F6 OSCILLATORIALES)M6Table Stichococcus(Chlorophyta Table1.1,212,234,260,311, 1.1,26Table1.2,59,320Table ULOTRICHALES)F,X16Table 312,325 7.1,341,404 1.1 RhodomonaslensPascheret Spondylosium(Chlorophyta Surirella(Bacillariophyta RuttnerF35Table1.7 ZYGMEMATALES)F,P6Table BACILLARIALES)F341,344 Richiella(Cyanobacteria, 1.1,273 Synechococcus(Cyanobacteria OSCILLATORIALES)M166,305 Staurastrum(Chlorophyta CHROOCOCCALES)M/F6Table ZYGMEMATALES)F6Table1.1, 1.1,11,20Table1.1,26Table Scenedesmus(Chlorophyta, 24,51,129,202,232,326,336, 1.2,97,155,165,181,183,184 CHLOROCOCCALES)F6Table 338,340,415 Table5.0,186,203Table5.2, 1.1,67,182,195,211,269,270, StaurastrumbrevispinumWestF,P 269, 277 Table 6.3, 305, 306, 320Table7.1,324,339,341, 57Table2.4 320 Table 7.1, 326 344 Staurastrumchaetoceras(Schroder)¨ Picoplanktic Z,free cells of ‘‘Scenedesmusquadricauda(Turpin) G.M.Sm.F,P201 Aphanocapsa. Larger species in Brébisson’F,JOft-recorded Staurastrumcf.cingulum(W.et Cyanothece speciesisnolongerregardedas G.S.West)F,P247 Synechocystis (Cyanobacteria anentityandisbeing StaurastrumdorsidentiferumW.et CHROOCOCCALES) M/F 6 Table subdivided(Johnetal.,2002)20 G.S.WestF,P328 1.1, 26 Table 1.2, 269 Table1.1,26Table1.2,60,157 StaurastrumlongiradiatumW.et Several species, all colonial; F, K?; Table4.2,195,277Table6.3, G.S.WestF,P?219 free cells are picoplanktic 424 StaurastrumpingueTeilingF,P20 Cyanobium, Z Scherfellia(Prasinophyta Table1.1,26Table1.2,195,201, Synechocystis limnetica Popovskaya CHLORODENDRALES)F6Table 219Table5.4,228,229,320 322 1.1 Table7.1,333 Synedra (Bacillariophyta Scourfieldia(Prasinophyta Staurodesmus(Chlorophyta BACILLARIALES) F 7 Table 1.1, SCOURFIELDIALES)M6Table ZYGMEMATALES)F6 62, 192, 233, 328, 344 1.1,425 Table1.1,129,203Table5.2, Synedra acus 54 Table 2.3, 320 Scrippsiella(Dinophyta 233,293,320Table7.1,325, Table 7.1, 338 PERIDINIALES)M312 331,385 Synedra filiformis Grun. F, D INDEX TO GENERA AND SPECIES OF PHYTOPLANKTON 519

Synedraulna(Nitzsch)Ehrenb.F,B Thalassiosira punctigera (Castracene) 213, 228, 229, 231, 292, 320 20Table1.1,322 Hasle M 130 Table 7.1, 323, 325, 328, 330 Synura(ChrysophytaSYNURALES)F Thalassiosira subtilis Ostenf. M 309 Uroglena americana Calkins F, U 7Table1.1,231,232,320Table Thalassiosira weissflogii (Grun.) 326, 328 7.1,321Table7.1,343 Fryxell et Hasle M (formerly Uroglena lindii Bourrelly F, U 20 SynurapeterseniiKorshikovF,W1 known as Thalassiosira fluviatilis) Table 1.2 130 35 Table 1.7, 54 Table 2.3, 60, Urosolenia (Bacillariophyta SynurauvellaEhrenb.F,E331 130 BIDDULPHIALES) F 7 Table 1.1, Thalassiothrix (Bacillariophyta 129, 232, 320 Table 7.1, 328, Tabellaria(Bacillariophyta BIDDULPHIALES) M 307 336, 385 BACILLARIALES)F7Table1.1, Thalassiothrix longissima Cleve et Uroslenia eriensis (H. L. Smith) 293,320Table7.1,325,329, Grun. M 307 Round et Crawford F, A 203 330 Thiocystis (Anoxyphotobacteria)F6 Table 5.2, 323, 331, Tabellariafenestrata(Lyngb.)Kutz.¨ Table 1.1 335 F,P?233,323 Thiopedia (Anoxyphotobacteria)F6 Tabellariaflocculosa(Roth.)Kutz¨ .F, Table 1.1 Volvox (Chlorophyta VOLVOCALES) F N29Table1.3,54Table2.3, Trachelomonas (Euglenophyta 6 Table 1.1, 12, 68, 83, 179, 205, 233,323,332,333 EUGLENALES) F 6 Table 1.1 211, 216, 285, 292, 294, 320 Tabellariaflocculosavar. Trachelomonas hispida (Perty) Stein Table 7.1, 343 asterionelloides(Grun.)Knuds.F, F, X2 15 Fig 1.2 Volvox aureus Ehrenb. F, G 26 Table N6Table1.1,20Table1.1,61 Trachelomonas volvocina Ehrenb. F, 1.2, 157 Table 4.2, 182, 184 Table2.5,64,184Table5.0,247 W2 321 Table 7.1 Table 5.0 Tetraedron (Chlorophyta, Treubaria (Chlorophyta Volvox globator Linnaeus F, G 20 CHLOROCOCCALES) F 324 CHLOROCOCCALES) F 352 Table 1.2 Tetrastrum (Chlorophyta, Tribonema (Xanthophyta CHLOROCOCCALES) F 6 Table TRIBONEMATALES) F 6 Table Westella (Chlorophyta 1.1, 51 1.1, 12, 320 Table 7.1, 324 CHLOROCOCCALES) F 352 Thalassionema (Bacillariophyta Trichodesmium (Cyanobacteria Willea (Chlorophyta BIDDULPHIALES) M 307, 311 OSCILLATORIALES) M 6 Table CHLOROCOCCALES) F 203 Table Thalassionema nitzschioides (Grun.) 1.1, 26 Table 1.2, 81, 166, 169, 5.2 Mereschkowsky M 307, 309, 203 Table 5.2, 234, 305, 306, Woloszynskia (Dinophyta 310, 311 316, 385 GYMNODINIALES) F, X2 7 Table Thalassiosira (Bacillariophyta Trichodesmium thiebautii Gomont M 1.1 BIDDULPHIALES) M 7 58, 166 Woronichinia (Cyanobacteria Table 1.1, 60, 67, 271, 307, 311, Tychonema (Cyanobacteria CHROOCOCCALES) F 6 Table 314, 317 OSCILLATORIALES) F 6 Table 1.1, 24, 26 Table 1.2, 81, 166, Thalassiosira baltica Grun. M 312 1.1, 26 Table 1.2 233, 272, 320 Table 7.1, 325, Thalassiosira decipiens (Grun.) Tychonema bourrellyi F, S1 115 332, 338, 401 Jørgensen M 311 Woronichinia naegeliana (Unger) Thalassiosira fluviatilis (syn. T. Umbellosphaera (Haptophyta Elenkin F, LO (formerly weissflogii) q.v. COCCOLITHOPHORIDALES) M 7 Gomphosphaeria naegeliana and Thalassiosira hyalina Grun. M 311 Table 1.1, 203 Table 5.2, 305, Coelosphaerium naegelianum) 248 Thalassiosira nordenskioeldii Cleve M 306, 309, 333 234, 307, 310, 311, 312 Uroglena (Chrysophyta Xanthidium (Chlorophyta Thalassiosira pseudonana Hasle et CHROMULINALES) F 7 Table 1.1, ZYGNEMATALES) F, N 6 Table Heindal M 35 Table 1.7 24, 83, 129, 130, 203 Table 5.2, 1.1 Index to genera and species of organisms other than phytoplankton

Abramis Actinopterygii, Blastocladiella Fungi, Blastocladiales Chydorus Crustacea, Cladocera 254 Cypriniformes 422 293 Table 6.1, 261, 266 Table 6.2, Acanthometra Rhizopoda, Radiolaria Bodo Zoomastigophora 252 Table 279, 287 252 Table 6.1 6.1, 259 Chydorus sphaericus 261, 266 Table Acartia Crustacea, Calanoidea 261, Boeckella Crustacea, Calanoidea 255 6.2, 279 262 Table 6.1, 336 Chytridium Fungi, Chytridiales 293 Acartia clausi 262 Boeckella gracilipes 336 Ciona Urochorda, Ascidacea 258 Acartia longiremis 261 Bosmina Crustacea, Cladocera 254 Table 6.1 Acineta Ciliophora, Suctoria 252 Table 6.1, 266 Table 6.2, 282, Clavelina Urochorda, Ascidacea 258 Table 6.1 287 Table 6.1 Actinophrys Rhizopoda, Heliozoa 252 Bosmina longirostris 266 Table 6.2 Clio Mollusca, Gastropoda 256 Table Table 6.1 Brachionus,Rotatoria, Monogononta 6.1 Aeromonas Bacteria, Vibrionaceae 253 Table 6.1, 259, 266 Table Clupea Actinopterygii, Clupeiformes 162 6.2, 281 261, 263, 427 Agrostis Angiospermae, Glumiﬂorae Brachionus calyciflorus 266 Table Clupea harengus 261, 427 335 6.2, 281 Coleps Ciliophora, Spirotricha 259 Alburnus Actinopterygii, Bythotrephes Crustacea, Cladocera Colpoda Ciliophora, Holotricha 252 Cypriniformes 422 254 Table 6.1, 261, 290 Table 6.1 Alosa Actinopterygii, Clupeiformes Calanus Crustacea, Calanoidea 255 Conochilus Rotatoria, Monogononta 290 Table 6.1, 261, 428 253 Table 6.1 Alosa pseudoharengus 290 Calanus finmarchius 261 Convoluta Platyhelminthes, Apherusa Crustacea, Malacostraca Canthocamptus Harpacticoidea 255 Turbellaria 253 Table 6.1 255 Table 6.1 Table 6.1 Coregonus Actinopterygii, Arcella Rhizopoda, Foraminifera 252 Carchesium Ciliophora, Peritricha Clupeiformes 289 Table 6.1 252 Table 6.1 Coregonus artedii 289 Argulus Crustacea, Branchiura 255 Carcinus Crustacea, Malacostraca 256 Cortaderia Angiospermae, Table 6.1 Table 6.1 Glumiﬂorae 335 Artemia Crustacea, Anostraca 254 Centropages Crustacea, Calanoidea Craspedacusta Coelenterata, Table 6.1, 269 255 Table 6.1, 261, 262, 282 Trachylina 253 Table 6.1 Asellus Crustacea, Isopoda 391 Centropages hamatus 261 Cyanea Coelenterata, Scyphozoa 253 Asplanchna Rotatoria, Monogononta Centropages typicus 262 Table 6.1 253 Table 6.1, 281 Cephalodella Rotatoria, Monogononta Cyclops Crustacea, Cyclopoidea 260 Asplanchna priodonta 281 292 Cyclops vicinus 260 Asterias Echinodermata, Asteroidea Ceratophyllum Angiospermae, Cyprinus Actinopterygii, 257 Table 6.1 Ranales 419 Cypriniformes 422 Asterocaelum Rhizopoda, Amoebina Ceriodaphnia Crustacea, Cladocera Cyprinus carpio 422 252 Table 6.1, 294 254 Table 6.1, 261, 277, 287 Cypris Crustacea, Ostracoda 254 Aurelia Coelenterata, Scyphozoa 253 Cetorhinus Selachii, Euselachii 263 Table 6.1 Table 6.1 Chaetonotus Gastrotricha 253 Cytophaga Bacteria, Cytophagales Australocedrus Gymnospermae, Table 6.1 142 Coniferae 335 Chaoborus Arthropoda, Diptera 256 Table 6.1, 269 Daphnia Crustacea, Cladocera 86, Bacillus Bacteria, Bacillales 162 Chara Chlorophyta, Charales 419 221, 254 Table 6.1, 261, 265, Balanus Crustacea, Cirripedia 255 Chirocephalus Crustacea, Anostraca 266, 266 Table 6.2, 267, 269, Table 6.1 254 Table 6.1 270, 274, 276, 277, 277 Table Beroë Coelenterata, Nuda 253 Table Chironomus Arthropoda, Diptera 6.3, 279, 280, 282, 284, 285, 286, 6.1 422 287, 289, 290, 299, 359, 390, Bicosoeca Zoomastigophora 252 Table Chironomus anthracinus 422 392, 404, 409, 418, 421, 422 6.1, 259 Chironomus plumosus 422 Daphnia cucullata 261, 287

520 INDEX TO GENERA AND SPECIES OF ORGANISMS OTHER THAN PHYTOPLANKTON 521

Daphnia galeata 221, 261, 266, 266 Euphausia tricantha 263 Keratella cochlearis 259, 281 Table 6.2, 267, 269, 276, 284, Euplotes Ciliophora, Spirotricha 252 Keratella quadrata 259, 281 287, 289 Table 6.1, 269 Daphnia hyalina 261, 266 Eurydice Crustacea, Malacostraca 255 Lates Actinopterygii, Perciformes Table 6.2 Table 6.1 263, 264, 341 Daphnia lumholtzi 261 Eurytemora Crustacea, Calanoidea Lates niloticus 341 Daphnia magna 261, 266, 277, 421, 255 Table 6.1 Lepomis Actinopterygii, Perciformes 422 Evadne Crustacea, Cladocera 254 Lepomis cyanellus 422 Daphnia pulex 266, 270 Table 6.1, 262 Leptodiaptomus Crustacea, Daphnia pulicaria 261, 277, 289, Calanoidea 409 290, 418 Festuca Angiospermae, Glumiﬂorae Leptodora Crustacea, Cladocera 254 Daphnia schoedleri 266 335 Table 6.1, 261 Diaphanosoma Crustacea, Cladocera Filinia Rotatoria, Monogononta 253 Leptomysis Crustacea, Malacostraca 254 Table 6.1, 409, 421 Table 6.1, 281 255 Table 6.1 Diaptomus Crustacea, Calanoidea Filinia longiseta 281 Limacina Mollusca, Gastropoda 256 266 Table 6.2, 389 Fitzroya Gymnospermae, Coniferae Table 6.1 Diaptomus oregonensis 266 Table 6.2 335 Limnocnida Coelenterata, Trachylina Flavobacterium Bacteria 142, 162 253 Table 6.1 Diastylis Crustacea, Malacostraca 255 Flustra Ectoprocta 257 Limnothrissa Actinopterygii, Table 6.1 Table 6.1 Clupeiformes 263, 264, 392 Difflugia Rhizopoda, Foraminifera Fulica Aves, Gruiformes Limnothrissa miodon 263, 264, 252 Table 6.1 Fulica atra 422 392 Dinophysis Dinophyta 252 Littorella Angiospermae, Campanales Table 6.1 Gadus Actinopterygii, Gadiformes 419 Doliolum Urochorda, Thaliacea Gadus morhua 427 Lobelia Angiospermae, Campanales 258 Table 6.1 Gammarus Crustacea, Amphipoda 419 Dreissena Mollusca, 389, 391 Loligo Mollusca, Cephalopoda 256 Lamellibranchiata 256 Table Gastrosaccus Crustacea, Malacostraca Table 6.1, 264 6.1, 323 255 Table 6.1 Lolium perenne Angiospermae, Dreissena polymorpha 323 Gigantocypris Crustacea, Ostracoda Glumiﬂorae 383 254 Table 6.1 Echinus Echinodermata, Echinoidea Globigerina Rhizopoda, Foraminifera Macrohectopus Crustacea, 257 Table 6.1 252 Table 6.1 Malacostraca 255 Table 6.1 Ensis Mollusca, Lamellibranchiata Megalogrammus Actinopterygii, 256 Table 6.1 Halteria Ciliophora, Spirotricha 252 Gadiformes 427 Eodiaptomus Crustacea, Calanoidea Table 6.1 Megalogrammus aeglifinus 287 Hertwigia Rotatoria, Monogononta 427 Eodiaptomus japonicus 287 292 Mesocyclops Crustacea, Cyclopoidea Epistylis Ciliophora, Peritricha 252 Holopedium Crustacea, Cladocera 254 254 Table 6.1, 260 Table 6.1 Table 6.1 Mesocyclops leuckarti 260 Escherichia Bacteria, Entobacteriacae Holothuria Echinodermata, Mesodinium Ciliophora, 49, 155, 158, 181 Holothuroidea 258 Table 6.1 Rhabdophorina 68 Escherichia coli 49, 155, 158, 181 Hydra Coelenterata, Hydrida 253 Metopus Ciliophora, Spirotricha 252 Esox Actinopterygii, Mesichthyes 422 Table 6.1 Table 6.1 Hydractinia Coelenterata, Microstomum Platyhelminthes, Esox lucius 422 Anthomedusae 252 Table 6.1 Turbellaria 253 Table 6.1 Eudiaptomus Crustacea, Calanoidea Moina Crustacea, Cladocera 254 255 Table 6.1, 266 Table 6.2, Isoetes Pteridophyta, Isoetales 419 Table 6.1 279, 280, 286, 390 Monas Zoomastigophora 252 Table Eudiaptomus gracilis 266 Table 6.2, Kellicottia Rotatoria, Monogononta 6.1, 259 280, 390 253 Table 6.1, 281 Monosiga Zoomastigophora 252 Euphausia Crustacea, Malacostraca Kellicottia longispina 281 Table 6.1, 259 256 Table 6.1, 263 Keratella Rotatoria, Monogononta Morone Actinopterygii, Perciformes Euphausia frigida 263 253 Table 6.1, 259, 281, 287 428 522 INDEX TO GENERA AND SPECIES OF ORGANISMS OTHER THAN PHYTOPLANKTON

Mulinum Angiospermae, Umbellales Penilia Crustacea, Cladocera 262 Salmo 389 335 Peranema Zoomastigophora 252 Salmo trutta 389 Myriophyllum Angiospermae, Table 6.1 Salpa Urochorda, Thaliacea 258 Myrtales 419, 422 Perca Actinopterygii, Perciformes Table 6.1 289, 290 Salpingooeca Zoomastigophora 252 Mysis Crustacea, Malacostraca 255 Percaflavescens 290 Table 6.1 Table 6.1 Percafluviatilis 289 Salvelinus Actinopterygii, Najas Angiospermae, Najadales Petromyzon Agnatha, Cyclostomata Clupeiformes 290 419 290 Salvelinus namaycush 290 Nassula Ciliophora, Holotricha 252 Petromyzon marinus 290 Schoenoplectus Angiospermae, Table 6.1, 259 Phoronis Phoronidea 257 Table 6.1 Cyperales 419 Nebaliopsis Crustacea, Malacostraca Phragmites Angiospermae, Scomber Actinopterygii, Perciformes 255 Table 6.1 Glumiﬂorae 419 261 Nitella Chlorophyta, Charales Physalia Coelenterata, Siphonophora Scomber scombrus 261 419 253 Table 6.1 Sialis Arthropoda, Megaloptera 256 Noctiluca Dinophyta 251, 252 Pleurobrachia Coelenterata, Table 6.1 Table 6.1 Tentaculata 253 Table 6.1 Sida Crustacea, Cladocera 254 Table Nothofagus Angiospermae, Fagales Pleuronema Ciliophora, Holotricha 6.1, 421 335 252 Table 6.1, 259 Simocephalus Crustacea, Cladocera Notholca Rotatoria, Monogonta 253 Plumularia Coelenterata, 254 Table 6.1, 261, 421 Table 6.1 Leptomedusae 252 Table 6.1 Sphagnum Bryophyta, Sphagnales Notonecta Arthropoda, Hemiptera Podochytrium Fungi, Chytridiales 424 263 293 Sphingopyxis Bacteria 142 Nyctiphanes Crustacea, Malacostraca Podon Crustacea, Cladocera 254 Sphyraena Actinopterygii, 256 Table 6.1 Table 6.1, 262 Perciformes 428 Polyarthra Rotatoria, Monogonta 259, Squilla Crustacea, Malacostraca 255 Obelia Coelenterata, Leptomedusae 281, 287 Table 6.1, 263 252 Table 6.1 Pontomyia Arthropoda, Diptera 256 Stentor Ciliophora, Spirotricha 252 Oikopleura Urochorda, Larvacea 258 Table 6.1 Table 6.1 Table 6.1, 259 Potamogeton Angiospermae, Stolothrissa Actinopterygii, Oithona Crustacea, Cyclopoidea 254 Najadales 419, 420 Clupeiformes 263, 264, 392 Table 6.1 Prorodon Ciliophora, Holotricha 252 Stolothrissa tanganicae 263, 392 Ophiura Echinodermata, Table 6.1, 259 Strobilidium Ciliophora, Spirotricha Ophiuroidea 257 Table 6.1 Protoperidinium Dinophyta 252 Table 252 Table 6.1, 259 Oreochromis Actinopterygii, 6.1 Strombidium Ciliophora, Spirotricha Perciformes 341 Pseudopileum Fungi, Chytridiales 293 252 Table 6.1, 259, 340 Oreochromis niloticus 341 Pyrosoma Urochorda, Thaliacea 258 Synchaeta Rotatoria, Monogonta 253 Ostrea Mollusca, Lamellibranchiata Table 6.1 Table 6.1, 259 256 Table 6.1 Oxyrrhis Dinophyta 251, 252 Table Quercus Angiospermae, Fagales 331, Temora Crustacea, Calanoidea 255 6.1, 270 359 Table 6.1, 261, 282 Temora longicornis 261 Palinurus Crustacea, Malacostraca Rhizophydium Fungi, Chytridiales Thiobacillus Bacteria, Chromatiaceae 256 Table 6.1 293, 294, 295 162 Patella Mollusca, Gastropoda 256 Rhizophydium planktonicum emend Thiobacillus denitrificans Table 6.1 293 162 Pelagia Coelenterata, Scyphozoa 253 Rhizosiphon Fungi, Chytridiales 293 Thunnus Actinopterygii, Perciformes Table 6.1 Rozella Fungi, Chytridiales 294 428 Pelagonemertes Nemertea 253 Table Rutilus Actinopterygii, Tintinnidium Ciliophora, Spirotricha 6.1 Cypriniformes 278, 422 252 Table 6.1, 259 Pelagothuria Echinodermata, Rutilus rutilus 278, 422 Tomopteris Annelida, Polychaeta 253 Holothuroidea 258 Table 6.1 Table 6.1, 263 Pelomyxa Rhizopoda, Amoebina 252 Sagitta Chaetognatha 256 Trichocerca Rotatoria, Monogonta 253 Table 6.1 Table 6.1 Table 6.1 INDEX TO GENERA AND SPECIES OF ORGANISMS OTHER THAN PHYTOPLANKTON 523

Tropocyclops Crustacea, Cyclopoidea Velella Coelenterata, Siphonophora Zostera Angiospermae, Najadales 254 Table 6.1 253 Table 6.1 420 Typha Angiospermae, Typhales 419 Vibrio Bacteria, Vibrionaceae 158, Zygorhizidium Fungi, Chytridiales 162 293, 294 Vampyrella Rhizopoda, Amoebina Vorticella Ciliophora, Peritricha 252 Zygorhizidium affluens 294 294 Table 6.1 Zygorhizidium planktonicum 293 General index

absolute viscosity, 44 Arrhenius coefficient, 107 bacteriochlorophylls, 5, 6 Table 1.1 accessory pigments, 10, 12, 13, 25, Arrhenius temperature scale, 186 bacteriophages, 295 95, 115, 193 arrow worms (chaetognaths), 256 bacterioplankton, 2, 140, 141; acetylene-reduction assay of Table 6.1, 263 concentrations and daily nitrogenase activity, 164 artificial neural networks (ANN), production rates, 141 Table 3.4; ‘acid rain’, 423 235 definition of, 2 acidification of natural waters, 423; ascendency, 303, 355, 357 bacterivorous phytoplankton, 131, reversal by adding phosphorus, ascidaceans, 258 Table 6.1 141 425;reversal by liming, 425 ‘ascidian tadpole’, 258 Table 6.1 bacterivory in algae, 159 Actinopterygii, 258 Table 6.1 ascorbate, 123 barium, 167 adaptive traits in phytoplankton, ash content of phytoplankton, 25, barnacles, 255 Table 6.1 207 26 Table 1.2, 27 barracuda (Sphyraena), 428 ADP (adenosine diphosphate), 99 assembly rules for phyoplankton basking shark (Cetorhinus), 263 advective patchiness, 87 communities, 362, 362 Table 7.8 bicarbonate transport, 128 aestivation, 59 atelomictic lakes, 74, 342 bicosoecids, 251 aeolian deposition, 170 atomic-absorption spectroscopy, 167 Biddulphiales (centric diatoms), 7 affinity adaptation of nutrient atmospheric carbon-dioxide Table 1.1, 13 uptake, 157, 194, 202, 203 invasion in, 127 bioassays, 169 airborne remote sensing, 134 ATP (adenosine triphosphate), 5, 95, biochemical oxygen demand (BOD), akinetes, 216, 249 99; phosphorylation by, 148, 149 297 alder flies (Megaloptera), 256 Table Auftrieb, 3 biodiversity, 368 6.1 Aufwuchs, 419, 420 biologically available phosphorus alewife (Alosa pseudoharengus), 290 autopoesis; (see also (BAP), 153, 154 Table 4.1, 155, 398 alkaline phosphatase, 155, 159 ‘self-organisation’ of biomanipulation, 263, 416 alkalinity, 124 communities), 355 biomineral reinforcement of cell allogenic vs. autogenic drivers of auxospore, 60, 64 structures, 27 change in species composition, Avogadro number, 95 bioturbation, 250, 413 360 avoidance reactions, 122 birds, 1, 76, 84 alternative steady states in shallow bivalves (lamellibranchs), 243, 256 lakes, 343, 382, 417, 421;forward Bacillariales (pennate diatoms), 7 Table 6.1, 290 and reverse switching, 421, 423; Table 1.1, 13 bleak (Alburnus), 422 influence of fish, 421;role of bacillariophytes; (see also diatoms); Blelham Enclosures, 217, 220, 226, zooplankton, 421 density of, 53, 55; deposition of 245, 274, 284, 284 Table 6.4, 299, aluminium, 424 silica, 182, 245;evolution of, 13; 357, 366, 370, 373, 374 amino acids, 123 growth limitation through silicon bloom, 56;inthe Kattegat, 1988, amoebae, 252 Table 6.1, 259 deficiency, 196; intervention in 312 amphipods, 263 silicon cycling by, 174; ‘bloom-forming’ Cyanobacteria, 401 anatoxins, 403 mixed-depth threshold for blue-green algal blooms, 401 annelids, 253 Table 6.1 growth, 80, 244; pigmentation bodonids, 251 anoxygenic photosynthesis, 5 variability in, 115; primary boron, 28 anoxyphotobacteria, 5, 6 Table 1.1 evolutionary strategies of, 234; bosminids, 261, 279 anthropogenic impacts, on food silicon content of, 28, 29 Table bottom deposits, sampling the webs, 290, 426;onpelagic 1.3, 31 Table 1.5, 53, 220; silicon superficial layer of, 220 systems, 395 requirements of, 27, 173, 197; bottom–up and top–down processes, antioxidants, in photosynthesis, 123 silicon uptake by, 28, 174; 250, 287, 288, 416 apatite, 151 structure of, 13 boundary layer, around a plankter, apoptosis, 297 Bacteria, 2, 5, 140, 158, 164, 170, 147, 148 aquo polymers, 39 264, 277 Table 6.3, 388, 392 branchiopods, 254 Table 6.1, 260 archaeans, 5, 93 bacterial pathogens, 292, 295 bream (Abramis), 422, 423

524 GENERAL INDEX 525

brown tides, 407 limitation of photosynthesis by, chaetognaths, 256 Table 6.1, 263 bryophytes, 11 127, 130; limitation of Chaetophorales, 12 bryozoans, 353 phytoplankton growth by, 30; chain formation, 60 buoyancy regulation, through ionic metabolic turnover of, 127; chaoborines, 256 Table 6.1 balance, 55;inCyanobacteria, 56, pelagic animal content of, 281; chaotic behaviour, 396 58 recycling of, in aquatic systems, Charales, 12 buoyant forces in water masses, 72 391;requirement of for algal cell chelates, 168, 169 burgundy blood alga, 115 doubling, 146, 188; sources of, 3 chemiluminescence, 167 carbon dioxide; atmospheric chitin, 60 C4 carbon fixers, 98 content of, 14; concentrations in chloride, algal requirement for, 172 C-, S- and R- primary evolutionary water, 124; depletion in chlorine, 28 strategies, 209, 210 Table 5.3, 212, photosynthesis, 96, 98, 126;asa Chlorobiaceae, 6 Table 1.1, 193 231, 233, 234, 298, 315; ecological factor regulating species Chlorococcales, 6 Table 1.1, 12 traits of C strategists, 352, 357, composition, 13; flux from Chlorodendrales, 6 Table 1.1, 11 370; ecological traits of S atmosphere to water, 127, 132; Chloromonadales, 6 Table 1.1 strategists, 359 supersaturating concentrations chlorophyll a, occurrence in algae, CS, CR, RS intermediate strategies, of, 126; uptake by phytoplankton, 5, 6 Table 1.1, 7 Table 1.1, 12, 13, 210 127 25, 26 Table 1.2, 95; algal content CSR triangle, 210, 232, 315, 363, carbonic anhydrase, 130 of, 33, 35 Table 1.7, 36, 37, 113;as 364, 396, 408 carboxylation, 94, 99, 127 aproxy of algal biomass, 34; calanoids, 254 Table 6.1, 260, 261, carboxylic acid, 100 relative to cell carbon, 114, 125 279 carotenoids, 25, 95, 123 chlorophyll b,occurrence in algae, 6 calcium, 28; algal requirement for, carp (Cyprinus carpio), 422, 423 Table 1.1, 11, 95 171; ionic concentrations in the cell growth cycle, 179 chlorophyll c, occurrence in algae, 6 sea, 171;inlakes, 171 cell assembly, regulation of, 181 Table 1.1, 7 Table 1.1, 12, 13 calcium bicarbonate and DIC, 171 cell division, 180;inchlorophytes, chlorophyll concentration calcium carbonate in phytoplankton 182;indiatoms, 180, 182;in supported in relation to TP, 399 exoskeletons, 13, 25, 53 dinoflagellates, 180;in chlorophyll synthesis, 168 calcium carbonate scales, 25 prokaryotes, 181; light efficiency Chlorophyta; classification of, 6 calcium hardness, 171 of (r/I), 190, 206 Table 1.1; DIC requirements of, Calvin cycle, 94, 95, 96, 98, 99, 100 cell division rates; in culture, 183; 123, 129;evolution of, 11; CAMP receptor protein (CRP), 128, as a function of algal osmotrophy in, 131 181 morphology, 183;asafunction of chloroplast, 146 capacity, environmental carrying; of temperature, 186;inrelation to choanoflagellates, 13, 251 atmospheric carbon flux, 136;of fluctuating light intensity, 193;in Chromatiaceae, 6 Table 1.1, 193 available silicon, 202;ofthe relation to light income, 206;in chromatic adaptation, 115 nutrient resources, 152, 194;of relation to persistent low light chromatographic analysis, 167 PAR income, 138;ofphosphorus intensity, 192, 207;inrelation to chromophores, 123 availability, 159;ofprimary nitrogen deficiency, 195;in chromosomes, 179 production, 131, 134, 136, 138;as relation to nutrient deficiency, Chromulinales, 6 Table 1.1 set by mixed depth, 138;assetby 194, 200, 203, 204;inrelation to Chroococcales, 6 Table 1.1, 26 Table transparency, 117 Table 3.2 nutrient stoichiometry, 200; in 1.2 carapace gape of cladocerans, 260, situ, 219 Table 5.4;inrelation to chrysolaminarin, 7 Table 1.1 261, 280 phosphorus deficiency, 194;in Chrysophyta; classification of, 6 carbamylation, 99 relation to photoperiod, 189;in Table 1.1, 13; DIC requirements carbohydrate, 53 relation to resource interaction, of, 129; distribution and calcium carbon; algal content of, 28, 30, 32, 197;inrelation to resource hardness, 171;evolution of, 11, 12; 33, 33 Table 1.6, 35 Table 1.7, 36, supply, 188; maxima at 20 oC, mixotrophy in, 131; pigmentation 146;availability to photosynthetic 184 Table 5.1 variability in, 115; silicon organisms, 124, 125; bacterial cell quota, definition, 31;of requirements, 27;storage content of; concentration phosphorus, 31 products in, 25; vitamin mechanism, 128; external cell wall, 24, 27 requirements of, 170 subsidies of, to pelagic systems, centropomids, 263 chrysose, 7 Table 1.1 390;fixation in the plankton, 93; cephalopods, 1, 18, 256 Table 6.1 chydorids, 261, 279 526 GENERAL INDEX

chytrids, 66, 292 critical patch size, 88, 89 decomposition rates of algae, 297 ciliates, 252 Table 6.1, 259, 260, 261, crustaceans, 259; classification of, deep ‘chlorophyll maxima’ (DCM), 353, 354 254 Table 6.1 59, 83, 115, 192, 328 ciliophorans, 252 Table 6.1, 259 Cryptomonadales, 6 Table 1.1; density; of air, 46;ofcarbohydrates, cirripedes, 255 Table 6.1 osmotrophy in, 131; 53;ofdiatoms, 53, 55;of cisco (Coregonus artedii), 289 photadaptation in, 115 metabolic oils, 53;ofmucilage, 55 cladocerans, 254 Table 6.1, 260, 261, cryptophytes, evolution of, 12; ;ofnucleic acids, 53;of 354 morphology of, 6 Table 1.1, 25 phytoplankton, 51, 53, 54 Table Cladophorales, 12 ctenophores (sea combs and sea 2.3, 55;ofpolyphosphate bodies, climate change, 431 gooseberries), 253 Table 6.1, 263 53;ofproteins, 53; salinity clupeoids, 263, 389 cultural eutrophication, definition dependence of, 40;ofsilica, 53; coastal waters, phytoplankton of, of, 397 temperature dependence of, 40;of 233, 310 cultures, 167 water, 39 Table 2.1, 40 cobalt, 28, 167 cyanelles, 6 Table 1.1, 11 density gradients in water columns, coccoliths, 7 Table 1.1, 13, 25, 130 Cyanobacteria; buoyancy in, 56, 58, 72, 74, 75, 79, 204 coccolithophorids, evolution of, 13, 67, 81, 124; cytology of, 25; density stratification, 73, 75 14; morphology of, 7 Table 1.1, 25 classification of, 6 Table 1.1, 10, desmids, 6 Table 1.1, 12, 25; DIC coelenterates, 252 Table 6.1 26 Table 1.2;indeep chlorophyll requirements of, 129 Coleochaetales, 12 layers, 193; DIC requirements of, detergents as a source of P, 398 community assembly in the 130; distribution and calcium detritus, 419 plankton, 302 hardness, 171; enhanced diadinoxanthin–diatoxanthin community ecology of abundance with eutrophication, reaction, 123 phytoplankton, 302, 350 402;evolution of, 10, 11;gas diatoms; (see also bacillariophytes), compensation point (where vacuoles of, 24, 56; habits of, 10; 13; deposition of silica, 182, 245; photosynthetic gains and in relation to low DIN, 196; DIC requirements of, 129; maintenance losses are balanced), nitrogen fixation in, 164, 169, 398; evolution of, 27, 234;growth 16, 116, 118, 120 in relation to N : P ratio, 198; limitation though silicon competition, definition of, 152 overwintering of, 405;pH deficiency, 196; intervention in competitive exclusion principle (of tolerance in, 124, 425; silicon cycling, 174; mixed-depth Hardin), 203, 369 photoprotection in, 123; threshold for growth, 80, 244; compositional change in pico–microplanktic morphology of, 27; communities rate of, 367 transformation, 269;production photoprotection in, 123; settling condensates of assimilation, 6 Table of siderophores, 169;storage velocities of, 52, 66, 67, 245; 1.1, 7 Table 1.1, 25, 26 Table 1.2, products in, 25;structure of silicon content of, 28, 29 Table 189 photosynthetic apparatus, 96; 1.3, 31 Table 1.5, 32, 53, 220; constancy, 304 toxicity in, 56, 402, 403;‘warning’ silicon requirements of, 27, 173, Continuous Plankton Recorder concentrations, 1229 197; uptake of silicon, 174; (CPR), 307 cyanobacterial blooms, 401 vitamin requirements of, 170 contractile vacuoles, 25 cyanophages, 295 diatoms, centric, 6 Table 1.1, 25 convection, 52 cyanophycin,85 diatoms, pennate, 7 Table 1.1 coot (Fulica atra), 422, 423 cyclopoids, 254 Table 6.1, 260, 278 diatoxanthin, 6 Table 1.1, 12 copepods, 254 Table 6.1, 259, 260 cylindrical curves, 81 dilution functions, 240 copper, 28; algal requirement for, cysts, of dinoflagellates, 215 dimethyl sulphide (DMS), 173 167;toxicity of, 167 cytochrome, 96, 167, 168 dimethyl sulphonoproponiate copper sulphate, as an algicide, 167, cytoplasm, 25 (DMSP), 173, 307; algal 416 osmoregulation by, 173; coregonids, 389 DAPI (DNA-specific stain), 220 DMS–DMSP metabolism, corethrines, 256 Table 6.1 DCMU, 66 173 Coriolis force, 17, 42 DNA, 140, 146 dinitrogen reductase, 164 crabs (decapods), 256 Table 6.1, 263 DNA : cell carbon ratio, as an index dinoflagellates; adaptive radiation Craspedophyceae, 13 of DNA replication, 220 in, 13, 14; DIC requirements of, crepuscular habitats, 192 daphniids, features of, 261; habitats 129, 130;evolution of, 12, 13, 16; critical depth model (of Sverdrup), of, 261 mixotrophy in, 131; 119, 120 decapods, 256 Table 6.1, 263 photosynthesis in, 123; GENERAL INDEX 527

‘swimming’ velocities, 68; vitamin eddy spectrum, 17, 18, 38, 42, 48, exergy, 303, 356; fluxes of, 357, requirements of, 170 251 375 Dinophyta, 7 Table 1.1; dinophyte El Niño, 305, 309, 382 exoskeletons, 25, 27 zooplankters, 252 Table 6.1 electivity of predators, 278 exponential phase of population dipterans, 263 electrophoretic mobility, 67 growth, 183 disentrainment of phytoplankton, endemism among phytoplankton, extracellular production, 100, 140, 75, 123 353 239 disequilibrium explanations of endoplasmic reticulum, 25 eyespots, 12 species diversity, 369; consumer endosymbiosis, 11, 13, 15, 305 effects, 371; intermediate energy flow in pelagic systems, 387, factor limitation of capacity, 169 disturbances, 372, 374, 384; 388;relevance to structure, 393, faecal pellets, 288 pathogenic effects, 371; 427 ferredoxin, 96, 165, 168 resource-based competition, 371 engineer species, 382, 419 Fick’s diffusion laws, 127, 147 dispersal of plankton, 353 entrainability, 17 Ficoll, 51 dissipation of turbulence, 47 entrainment of phytoplankton, 38, filter-feeders, 260, 261, 262 dissipative ecological unit (DEU), 39, 67, 69, 74, 75, 204, 243 filter-feeding; on detrital POC, 277; 351, 355, 382 entropy, 355 impacts of, 264, 270, 274; dissolution of diatom frustules, 174 environmental grain, 47 intervention of planktivores, 277, dissolved humic matter (DHM), 142, environmental heterogeneity, 289; limiting food concentrations 390, 424 78 for, 265, 275, 277; measurement dissolved inorganic carbon (DIC), epilimnion, 75 of, 265; nutritional aspects, 270; 125; uptake in phytoplankton, 128 epilithic algae, 342 rates of, 265, 266, 274;inrelation epiphytes, 285 to food availability, 267;in dissolved inorganic nitrogen (DIN), equitability (evenness), 366 relation to temperature, 274; 163 ethylene diamine tetra-acetic acid saturating food concentrations dissolved organic carbon (DOC), 93, (EDTA), 168 for, 274, 276; size selection, 267; 139, 140, 141, 142, 261, 264, 388; Eubacteria, 5 in turbid water, 280 DOC produced by phytoplankton, Euglenales, 6 Table 1.1 filtering setae of cladocerans, 260, 100, 124; DOC as a source of DIC, euglenoids, 12, 25 261 126 euglenophytes; classification, 6 fish, 1, 18 dissolved organic matter (DOM), Table 1.1;evolution of, 11, 12; fishing industry, 427 142 osmotrophy in, 131;storage fish-rearing ponds, 418 dissolved organic nitrogen (DON), products in, 25 fish-supportive capacity of pelagic 163 eukaryotes, 11; early evolution of, production, 389 disturbance, 304, 372 11, 12, 13 flagellates, 6 Table 1.1;vertical diversity indices, 366 euphausids, 256 Table 6.1, 263 distribution of, 83 doliolids, 258 Table 6.1, 262 euphotic zone, 116 flagellum, propulsion, 49 droop model of nutrient uptake, euplankton, 2 Flexibacteria, 5 150 Eustigmatophyta, 6 Table 1.1, 12 flood-plain lakes, 352 dry masses of phytoplankton, 25, 26 Eutreptiales, 6 Table 1.1 flow cytometry, 140 Table 1.2;inrelation to volume, eutrophic food webs, 140 fluorescence, 122;asasurrogate of 25 eutrophic lakes, phytoplankton of, biomass, 122;asasurrogate of ducks, 423 232 phyletic composition, 122 Dugdale model of nutrient uptake, eutrophication; of coastal waters, fluorometry, 52, 132 150 426;oflakes, 397;ofseas, 425;of flushing, 240 dugongs, 427 Windermere, 333;reversal of, fluvial ‘dead zones’, 242 dust deposition (aeolian deposition), 408 fluvioglacial deposits, 337 170 evaporative heat losses from water foamlines, 85, 86 bodies, 41 food chains of the pelagic, 261; echinoderms, 257 Table 6.1 evenness (or equitability), 366 energetic dissipation in, 291; ecological efficiency of energy excretion, of excess photosynthate, interactive linkage strength, 291; transfer, 261 123 length of, 291 ecological stoichiometry, 199, 262 excretory products of zooplankton, food location by chemoreception, ectoprocts, 257 Table 6.1 287 280 528 GENERAL INDEX

food requirements, of calanoids, grazing losses of phytoplankton, high-nutrient, iron-deficient areas of 262 220 the ocean, 170 of cladocerans,262;ofpelagic green tides, 407 Hill–Bendall model of fish, 389 greenhouse gases, oceanic photosynthesis, 94 food, zooplankton-supportive absorption of, 428 holopedids, 261 capacity of, 262 gross primary production (GPP), 141 holotrichs, 252 Table 6.1, 259 food-web control nodes, 394 growth rate; (see also replication horizontal patchiness of foraging in calanoids, 279;in rate), 178 phytoplankton, 84, 88 relation to pelagic energy flows, growth-regulating nucleotides, 158 human metabolites, as a source of 388; saturating food availability, growth and reproductive strategies P, 398 280; superiority over of freshwater phytoplankton, 208; humic acids, 168 filter-feeding, 279, 286, 394 correspondence with morphology, humic lakes, plankton of, 12, 326 foraminiferans, 252 Table 6.1, 211; C-, S- and R- primary hydrogen, algal content of, 28, 32, 259 evolutionary strategies, 209, 233, 33 Table 1.6 form resistance of phytoplankton 315; CS, CR, RS intermediate hydroxyapatite, 129 (to sinking), 50, 60; coefficient of, strategies, 210; SS strategy, 211, hydrozoans, 252 Table 6.1 51;ascontributed by chain 234; violent, patient and hyperparasitism, 294 formation, 60;asprovided by explerent strategies, 211 hyperscum, 215 protuberances and spines, 60;of guanosine bipyrophosphate (ppGpp), hypersensitiviy of hosts to parasitic stellate colonies, 63 158, 181, 214 attack, 294 friction velocity; (see also turbulent Gulf Stream (North Atlantic Drift hypnozygotes, 215 velocity), 46, 48 Table 2.2 Current), 289, 306 hypolimnion, 75 frictional drag coefficients, 41 Gymnoceratia, 216, 229 frustules; (see also diatoms, siliceous Gymnodiniales, 7 Table 1.1 ice cover, 306, 307, 308, 322 cell walls), 27, 32, 174 gymnodinioids, 13 information theory, 366 fucoxanthin, 6 Table 1.1, 7 Table 1.1, intermediate disturbance hypothesis 12, 13 HNLC oceans (high nitrogen, low (IDH), 373, 377 fulvic acids, 168 chlorophyll), 308 invasion by species ‘new to the fungal epidemics, 293 habitat filtration, 360 locality’, 384 fungi, 2; parasitic on algae, 292 habitat templates, 315, 348, 394 internal phosphorus loading, 412 haddock (Megalogrammus aeglifinus), ionic regulation, 55 Gaia principle, 173 427 iron, 167, 335, 398, 424; algal gasvacuoles, 56 Haeckel, E., 3 requirement for, 168; cell gasvesicles, 57, 58 Halobacteria, 5 contents of, 28, 168 gastropods, 256 Table 6.1 Haptonema, 13 complexes with organic carbon gastrotrichs, 253 Table 6.1 haptophytes; classification of, 7 (DOFE), 170; limitation of Gelbstoff, 111 Table 1.1;evolution of, 11, 13; nitrogen fixation, 169; limiting generation time, 178, 188 morphology of, 24; pigmentation concentrations, 168; sources of, germination of resting stages, 214, variability in, 115; vitamin 170; symptoms of cell deficiency, 229, 250 requirements of, 170 168; uptake by algae, 168 gill rakers, 263, 389 harmful algal blooms (HAB), 312, iron-binding chelates, 168 Gilvin, 111 401 IRONEX oceanic fertilisation, 170, glaciations, 336 heat flux, solar, 72 308 Glaucophyta, 6 Table 1.1 heleoplankton, definition of, 2 island biogeography, 352 global warming, 14 hemipterans, 263 isopycny, 19, 72, 82 glucose, 100 Henry’s law, 125, 126 glutathione, 123 Hensen, V., 3 jellyfish, 2 glycerol, 52 herbivory on phytoplankton, 250 Jenkin mud sampler, 249 glycogen, 6 Table 1.1, 25, 26 Table herring (Clupea harengus), 261, 263, 1.2, 59, 98, 189 427 kairomones, 269 glycolate excretion, 100, 239 heterocysts (heterocytes), 6 Table karyokinesis, 179 glycolic acid, 100, 123 1.1, 26 Table 1.2, 164, 196, 230 kataglacial lakes, phytoplankton of, Gonyaulacales, 7 Table 1.1 heterotrophy, 12, 126, 141 232 gonyaulacoids, 13 Hibberdiales, 7 Table 1.1 Kelvin–Helmholtz instability, 79 GENERAL INDEX 529

keystone species, 382, 394, 427 light-saturation of photosynthesis, manganese, 28, 167, 424; algal kinematic viscosity, 44, 48 103, 106 Table 3.1, 122, 136 requirement for, 167 KISS model of critical patch size, 88 limiting capacity, 152 mannitol, 6 Table 1.1 Kolmogorov eddy scale, 42, 45 limiting factors, 151 mantis shrimps, 263 krill (euphausids), 256 Table 6.1, 263 limnoplankton,, 2 marine snow, 66, 166, 248, 249, 430 lipid, 6 Table 1.1, 7 Table 1.1, 54; marl lakes, 129 accumulation, 54 mass mortalities of phytoplankton, lake trout (Salvelinus namaycush), 290 lipo-polysaccharides, 403 214 lakes as a source of CO2, 390 Lloyd’s crowding index, 82 match–mismatch hypothesis, 290 lamellibranchs, 256 Table 6.1 lobsters (decapods), 256 Table 6.1, maturation-promoting factors (MPF), laminar flow, 44 263 181 Langmuir circulations, 85, 85 Lorenzian attractors, 396 mechanical energy loss in water larvaceans, 258 Table 6.1, 259 loss rates of phytoplankton, 139, columns, 47 larvae, planktic: actinotrocha, 257 239; aggregated, 297; due to cell medusae, 252 Table 6.1 Table 6.1;amphiblastulae, 252 death, 240, 296; due to megalopterans, 256 Table 6.1, 263 Table 6.1; appendicularia, 258 consumption by animals, 240, megaplankton, 263 Table 6.1; auricularia, 257 Table 243, 278, 280, 285, 286; due to Mehler reaction, 100, 123 6.1; bipinnaria, 285 Table 6.5; downstream transport, 239, 242; membrane transport systems, 148 cyphonautes, 257 Table 6.1; due to parasitism, 240, 292, 295; memory in community assembly, cypris, 255 Table 6.1; megalopa, due to sedimentation, 240, 243; 366, 380, 384 256 Table 6.1; nauplii larvae, 259; due to washout, 239, 240, 241; meromictic lakes, 74, 263 paralarvae, 264;phyllosoma, 256 from suspension, 70, 76; seasonal meromixis, 74, 340 Table 6.1; pilidium, 253 Table 6.1; variations, 297, 299 meroplankton, 2, 243 pluteus, 257 Table 6.1; losses, distinction between mesophytoplankton, size definition trochophore, 256 Table 6.1; physiological and demographic of, 5 trochosphere, 253 Table 6.1; processes, 239 mesotrophic lakes, phytoplankton veliger, 256 Table 6.1; zoea, 256 luxury uptake of nutrients, 31, 151, of, 233 Table 6.1 161, 194 mesozooplankto: of freshwaters, latent heat of evaporation, 41 Lycopodium spores, as a model of 260;ofthe sea, 261 Laurentian great lakes, 290 suspended phytoplankton, 76, 80, metalimnion, 75 leptodorids, 261 245 methanogens, 5 leucosin, 6 Table 1.1 Michaelis–Menten kinetics, 150 licensing factors, 181 mackerel (Scomber scombrus), 261 microalgae (µ-algae), 2, 4 Liebig’s law of the minimum, macroecology, 380 microbial food web, 140, 259, 261, 152 macroinvertebrates (of macrophyte 318 light (see also photosynthetically beds), 419 microbial ‘loop’, 140 active radiation), 95; absorption macrophytes, 342, 391, 395; microcystins, 403, 404 by water, 138; attenuation architecture of, 418;effects of micronutrients, inorganic, 166; (extinction) of, underwater, 103, eutrophication on, 420; leaf area organic, 170 109, 110, 113, 116;effect of cloud index in, 420;asrefuges for microphytoplankton, size definition on, 108; light underwater, 108, potamoplankton, 243 of, 5 110; surface incidence of, 108; macrophytoplankton, size definition microplanktic protists, 251 surface reflectance, 108 of, 5 microplanktic metazoans, 259 light harvesting by photosynthetic macroplanktic herbivores, 262 microstratification, 81 organisms, 94, 95, 123 macroplanktic predators, 261 microzooplankton, 170, 251, 259, light-harvesting complex (LHC); areal macrothricids, 261, 279 261, 287, 392 concentrations of, 137; mechanics magnesium, 28; algal requirement migration of phytoplankton, of, 96, 97, 192; numbers of, 113; for, 172;availability of, 172 vertical, 83 structure of, 95, 96 maintenance requirement of Milankovitch cycle, 431 light adaptation in phytoplankton, resource, 189 minimal communities, 351 113, 114, 120 mammals, 2, 18 minimum cell quota, of a given light-dependent growth in malacostracans, 255 Table 6.1 nutrient, 150 phytoplankton, 206 manatees, 427 Mischococcales, 6 Table 1.1 light : nutrient ratio in lakes, 199 Mandala, of Margalef, 314, 408 mitochondria, 25 530 GENERAL INDEX

mitosis, 180 nanophytoplankton size definition nutrient-induced fluorescent mixing times, 75, 76, 117 of, 5 transients (NIFT) indicative of P mixolimnion, 340 nekton, 1, 2, 18, 263 deficiency, 159 mixotrophy in phytoplankton, 131, nematodes, 253 Table 6.1 nutrient ratios, in algal tissue, 28 159 net primary production (NPP), 134; nutrient regeneration, 287 models simulating phytoplankton by global domains, 135 Table 3.3 growth and performance, 234 netplankton, 4 ocean; heat exchanges, 41;renewal Mollusca, 256 Table 6.1 niche, 303, 354 time, 39;totalarea of, 39;total molybdate-reactive phosphorus Nile perch (Lates), 341 volume of, 39;water circulation (MRP), 155, 399 Nile tilapia (Oreochromis), 341 in the, 41, 42 molybdenum, 28, 167, 335, 398; nitrate reductase, 163; synthesis of, oceanic fronts, 307, 308 algal requirement for, 167 168 oceanic provinces, 318 monimolimnion, 340 nitrilotriacetic acid (NTA), 168 Oedogoniales, 12 Monin–Obukhov length, 72, 79, 119, nitrogen; algal content of, 28, 30, oils (as storage product), 6 Table 1.1, 121, 243 32, 33, 33 Table 1.6, 35 Table 1.7, 7 Table 1.1, 25;effect on cell Monod equation, 150 36, 161;availability to densities, 53, 54 monosccharides, 100 phytoplankton, 162, 163; cell oligotrophic lakes, 388; Monosigales, 13 quotas of, 164; external phytoplankton of, 232 monosilicic acid, 28, 173, 182 concentrations favouring oligotrophic food webs, 140 monovalent : divalent cation ratio, dinitrogen fixers, 196; external open oceans, phytoplankton of, 172 concentrations half-saturating 233 morphological adaptations of phytoplankton growth, 196; operons, 149, 181 phytoplankton, 19, 23, 24, 48, 53, N-regulated capacity of opossum shrimps (mysids), 255 120 Patagonian lakes, 162, 196, 335; Table 6.1 motility, advantages of for potential chlorophyll yield, 164; organic composition of phytoplankters, 205, 206 requirement of for cell doubling, phytoplankton, 28 mucilage, presence of in plankters, 146, 188, 195; sources of, 162; orthophosphoric acid, 153 271;asadefence against uptake rates of algal cells, 163 Oscillatoriales, 6 Table 1.1, 26 Table digestion, 273;asadefence nitrogen fixation, 164;in 1.2 against grazers, 270, 273;asa Cyanobacteria, 164, 398; DIN osmoregulation, 25 defence against heavy metals, sensitivity of, 165, 196; osmotrophy, 131 273;asadefence against oxygen, dependence upon energy, 165; outgassing of CO2 from lakes and 273;for nutrient sequestration, dependence upon phosphorus, rivers, 126 272;production as a buoyancy 165;redox sensitivity of, 164; overwintering of Cyanobacteria, aid, 55, 67;properties of, 24, 55, requirement for trace metals, 214, 405 271;relative volume of, 57 Table 165 oxygen, algal content of, 28, 32, 33 2.4;asaresponse to nutrient nitrogenase, 168 Table 1.6 deficiency, 271;for North American Great Lakes, 89 self-regulation, 272;for NorthAtlantic Oscillation (NAO), pH, 124, 423 streamlining, 272 289 pH–CO2–bicarbonate system in mucilaginous phytoplankters, 24 northern cod (Gadus morhua), 427 water, 125 mucilaginous threads, 67 Nostocales, 6 Table 1.1, 26 Table 1.2 pH sensitivity of phosphate Muller,¨ J., 3 nucleus, 25; nuclear division solubility, 153 mycoplankton, 2, 2 (karyokinesis), 179 packaging effect on pigment mycosporine-like amino acids, 123 nucleic acids, 27, 53, 179 distribution, 192 mysids, 255 Table 6.1, 263 nutrients, 145;availability to paradox of the plankton (of myxomycetes, 295 phytoplankton, 145, 146; cell Hutchinson), 368, 379 quotas, 150, 199; demand versus paralarvae, 256 Table 6.1 NADP (nicotinamide adenine supply, 145, 188; flux rates to paramylon (or paramylum), 6 Table dinucleotide phosphate), 94, 96; cells, 147; intracellular sensitivity 1.1, 25, 98, 189 reduction of, 165 and control, 149; limitation, 151, parasites of phytoplankton, 292, 294 nannoplankton, 2 152; uptake by phytoplankton, parasitic fungi, 66 nanocytes, 215 145, 146, 148, 150; uptake, role of particulate organic carbon (POC), nanoflagellates, 259, 280, 287 motion, 147 126, 279, 390, 393 GENERAL INDEX 531

particulate organic matter (POM), photoheterotrophy, 5 phototrophic bacteria, 5 390 photoinhibition, 104, 117, 121, 122, phycobilins, 6 Table 1.1, 10, 12, 25, patchiness of phytoplankton, 78, 84, 124, 194, 246 26 Table 1.2, 168 88 photons, 95 phycobiliproteins, 115 Pavlovales, 7 Table 1.1 photon flux density (PFD), 95, 123 phycobilisomes, 10, 95 Péclet number (Pe), 147 photon interception and absorption, phycocyanin, 6 Table 1.1, 26 Table Pedinellales, 7 Table 1.1 95 1.2, 115, 193 Pedinomonadales, 6 Table 1.1, 11 photooxidation, 121 phycoerythrin, 6 Table 1.1, 26 Table penetrative convection, 72 photoprotection, 104, 121, 122, 194 1.2, 115, 193 perch (Percafluviatilis), 289 photorespiration, 99, 123, 139, 239 phycomycetes, 292 perennation of phytoplankton, 249 photosynthesis, as a basis of aquatic phycoviruses, 295 Peridiniales, 7 Table 1.1 production,, 5, 93; biochemistry phyllopods, 260, 279 peridinians, 32 of, 94; carbon limitation of, 127, Phytodiniales, 7 Table 1.1 peridinin, 13 130; carbon oxidation, 100;carbon phytoplankters, 3 peritrichs, 252 Table 6.1 sourcing in, 124, 125; condensates phytoplankton, definition of, 2, 3, Permian extinctions, 14 of, 25; electron transport, 94, 95; 36; functional classification of, 4; phaeophytes, 12 hexose generation, 94, 95; phyletic classification of, 4, 5, 36; phaeophytin, 96 Hill–Bendall model of, 94; general characteristics of, 16; phagotrophy, 12;inalgae, as a integration through depth, 104, numbers of species of, 4; size, 19, means of nutrient sequestration, 119, 132; integration through 20 Table 1.1, 34, 35 Table 1.7, 36, 159 time, 132; light efficiency of (P/ I), 53; shape, 19, 20 Table 1.1, 22, 23, phoronids, 257 Table 6.1 103, 105; light harvesting in, 94, 35 Table 1.7, 50;form resistance, phosphatase production in algae, 95; light saturation of, 103, 106 50, 53, 60, 243; morphological 159 Table 3.1, 122, 136; measurement, adaptation, 19, 23, 24, 48, 53, 120; phosphate binding in soils, 398 101, 105, 107; models of, 104, 110; turbulent embedding of, 48, 49; phosphoglycolate, 99 net of respiration, 107, 132; ‘swimming’, 49;effect of viscosity, phosphoglycolic acid, 123 oxygen generation, 94;productive 49; settling velocities of, 39, 49, phosphorus, algal content of, 28, 31, yields, 133, 139;quantum 50, 52, 61 Table 2.5, 67, 68, 75, 77; 32, 33, 33 Table 1.6, 36, 151; efficiency of, 95, 98, 100; as a function of size, 53;asa affinity adaptation, 157; reduction of CO2, 94, 96, 98, 146; function of density, 53;asa availability to phytoplankton, 398, reduction of water, 94;regulation function of chain formation, 62; 399; deficiency in cells, 158; by light, 101, 102, 108, 120, 121;in as a function of cylindrical external concentrations relation to depth, 103; surface elongation, 62;asafunction of half-saturating phytoplankton depression of, 104 colony formation, 63;stellate growth, 195;asafactor limiting photosynthetic inhibitors, 66 colonies, 63; settling velocities as growth rate of phytoplankton, photosynthetic pigments, 5, 6 Table a function of cell vitality, 65, 66; 158;fractions in water, 154 Table 1.1, 7 Table 1.1, 11, 12, 25, 26 entrainment of, 38, 39, 67, 69, 74, 4.1; minimum requirements of Table 1.2, 123 75, 77;vertical distribution of, 80, algae for, 151; potential photosynthetic quotient (PQ), 100, 83; horizontal patchiness of, 84, chlorophyll yield, 160;quotas 105, 107, 163, 190 88;dry masses of, 25, 26 Table 1.2; supporting replication, 158; photosynthetic rates, Tab 3.1, 104, densities of, 51, 53, 54 Table 2.3; requirement of for cell doubling, 106 Table 3.1;temperature organic composition of, 28; 146, 188, 194; sources of, 151; dependence of, 106 elemental composition, 24, 25, storage adaptation, 157; uptake photosynthetic yield to planktic 28, 35 Table 1.7, 36, 146; ratesofalgal cells, 150, 155, 157 food webs, 139 photosynthesis in, 93; light Table 4.2;velocity adaptation, 157 photosynthetically active radiation adaptation in, 113, 114, 120; phosphorus, recycling of, 412 (PAR); (see also light), 16, 95, 108; uptake of carbon in, 127, 128; phosphorus ‘release’ from carbon yield, 100; energy bacterivory in, 131;excretion in, sediments, 413 equivalence, 95, 100 123; nutrient requirements of, photadaptation, to low light doses, photosystem I, 94, 96, 122, 146; nutrient uptake, 19; 120, 193, 194 165 availability of nitrogen to, 164; photoautotrophy, 5, 94, 141 photosystem II, 94, 95, 122, nitrogen uptake rates of, 163; photodamage, 124 123 availability of phosphorus to, 153, photodegradation (of DOM), 143 phototrophy, 12 154, 154 Table 4.1, 398, 399 532 GENERAL INDEX

phytoplankton, definition of (cont.) oligotrophic lakes, 319;of Planck’s constant, 95 phosphorus; uptake rates of, 150, subarctic lakes, 328;ofalpine plasmalemma, 24, 25, 146 155, 157 Table 4.2; lakes, 329;ofthe English Lakes, planktivory, 392, 395 phosphorus-constrained growth 330;ofAuracanian lakes, 335;of plankton, definition of, 1, 2 of, 158; cell phosphorus quotas, kataglacial lakes, 336;ofthe plastids, 11, 12, 13, 25, 123 161;major-ion requirements of, African Great Lakes, 339;ofLake plastoquinone (PQ), 96, 122 171;astrophic-level indicators, Titicaca, 342;ofshallow lakes, plate tectonics, 309 129;growth and replication of, 342;inrelation to supportive polder lakes, 366 178;growthrates of, (see also cell capacity, 346;overview of polychaetes, 253 Table 6.1, 263 division rates), 183;asafunction mechanisms, 383 polymerase chain reaction (PCR), of nutrient availability, 151; phytoplankton population dynamics 140 light-dependent growth in, 206; in natural environments, 217; polymictic lakes, 74 areas projected by, 192; adaptive estimating in-situ rates of growth, polynia, 306 traits of, 207;growthand 217; episodic outbursts of rapid polyphemids, 261 reproductive strategies, 208; increase, 217; observed increase polyphosphate bodies, 53 strategies for survival of resource rates, 217;frequency of dividing polysaccharides, 98 exhaustion, 211; loss from cells (FDC), 218;frequency of Porifera (sponges), 27 suspension, 70, 76; losses to nuclear division, 220;from post-upwelling relaxation, 309 grazers, 139, 141, 220, 250; resource depletion, 220; spring potamoplankton, 2, 242 counter-grazing adaptations, 269; increase in a temperate lake, 221; potassium, 28; algal requirement effects of zooplankton selection effect of inoculum size, 223, 225, for, 172 on, 287; beneficial effects of 229;effect of nutrient availability, power, 303, 355 zooplankton, 287; selection by 223;effect of temperature, 223, Prasinophyta, 6 Table 1.1, 11 performance, 225; seasonality of 226;effect of underwater light Prasiolales, 12 selective mechanisms, 231; field, 223, 226;effect of resource prawns (decapods), 256 Table 6.1 eutrophic species of, 232; diminution, 223;effect of lake Prochlorales, 6 Table 1.1, 26 Table oligotrophic species, 203 Table enrichment on timing of 1.2 5.2, 232, 233;ofshallow lakes, maxima, 224; species selection by prochlorobacteria, 6 Table 1.1, 11, 233;ofcoastal waters, 233;of performance, 225; exploitative 26 Table 1.2 open oceans, 233;ofrivers, 242; efficiency, 225; comparison of programmed cell death, 297 entrainment criteria for, 243; species-specific performances, 226; projected area of algal shape, 192 sedimentary fluxes of, 247, 249, effect of light-exposure prokaryotes, 25 318; parasites of, 292, 294; thresholds, 226;inrelation to Prorocentrales, 7 Table 1.1 parasitic infections of, 66; phosphorus availability, 228;in PROTECH phytoplankton growth perennation of, 249;regenerative relation to pH, 228;inrelation to model, 236, 377, 383, 415 strategies of, 249;trait separation N:P ratio, 230;inrelation to proteins, 27, 53 of, 319; community assembly in, transparency, 230;inrelation to protistans, 2, 11, 27, 251 350; succession in the sea, 313; carbon dioxide, 231;inrelation to Protobacteria (α-), 142 biomass levels in the sea, 313, seasonality, 231, 232, 234; Protobacteria (γ -), 142 388; biomass levels in inland quantification in a Blelham protomonadids, 251 waters, 345; dispersal Enclosure, 221 Table 5.5, 221 proton motive forces, 148 mechanisms, 353;ofacidic Table 5.6;asinfluenced by protoplasm, 25, 30 waters, 423, 424;ofhumic lakes, simultaneous loss rates, 298; protozoans, parasitic on algae, 294 326; methods to control species selection by performance, Prymnesiales, 7 Table 1.1 abundance, 414 298;effect of inoculum size, 299; purple non-sulphur bacteria, 5 phytoplankton assemblages, sinking losses., 299; simulation pycnocline, 75, 79, 245, 340 communities and structure, 302; models of, 234 Pyramimonadales, 6 Table 1.1, 11 of high-latitude seas, 306, 308;of phytosociology, 318; application to pyrosomans, 262 theNorth Pacific, 304;ofthe the pelagic, 319 South Pacific, 306;ofoceanic Phytotelmata, 292, 352 Q10 ,ofphotosynthetic rate, 107;of upwellings, 308;ofcontinental picophytoplankton, size definition cell division, 186 shelves, 309, 310;ofinshore of, 5;settling velocities of, 68;in quanta, 95 waters, 317;oflarge oligotrophic oligotrophic oceans, 234 quantum efficiency of lakes, 319;ofsmall and medium plagioclimax, 370 photosynthesis, 95 GENERAL INDEX 533

quantum yield of photosynthesis, Richardson numbers, 73 sedimented material, resuspension 98, 100 Rift Valley lakes, 339;food webs of, of, 250 quinones, 96 263 seiching, 340 river bed roughness, 46 selective planktic feeding, 278; r-, K- and w- selection, 209, 212, 231, rivet theory (of Ehrlich and Ehrlich), impacts of, 280 314 382 ‘self-organisation’ of communities, radiolarians, 3, 27, 252 Table 6.1, RNA, 140, 146, 199, 262 355 259 roach (Rutilus rutilus), 278, 392, 422 seston, definition of, 2 rails, 423 rotifers, 253 Table 6.1, 259, 292, settlement of diatom frustules, 175 Raphidomonadales, 6 Table 1.1 354 settling flux, 220 Raphidophyta, 6 Table 1.1, 12 RUBISCO (ribulose 1, 5-biphosphate shallow lakes, characteristics of, raptorial feeders, planktic, 260, 278 carboxylase), 94, 95, 98, 99, 127, 319, 342, 391; alternative steady recruitment of larval fish, 289 128;asanoxidase, 99, 123, 140 states in, 343, 417;phytoplankton recycling of phosphorus, 412 RuBP (ribulose1, 5-biphosphate), 94, of, 233 recycling of resources in the 98, 99, 123 Shannon–Weaver index, 366, 378 pelagic, 288, 296 sharks, 427 Redfield stoichiometric ratio, 32, 33, salmonids, 389 shear, 148, 250, 413 33 Table 1.6, 37, 188, 198 salps, 258 Table 6.1, 261, 262 shear velocity; (see also turbulent red tides, 407 sampling strategies for velocity), 46, 48 Table 2.2 redox-sensitivity of phosphate phytoplankton, 89 shelf waters, 117 Table 3.2, 135, 309, solubility, 153;ofnitrogen saprophytes, 297 430 speciation, 162;ofnitrogen sarcodines, 259 Sherwood Number (Sh), 148 fixation, 164;totoxicity of metal satellite-borne remote sensing, 131, shortwave electromagnetic micronutrients, 167 134 radiation, 72 relocation of phosphorus capacity, saxitoxins, 403, 407 siderophores, 169 away from plankton, 411 scales, calcareous, 7 Table 1.1, 25; sidids, 260 replication rate, 178 siliceous, 25 sieve effect, 112 reptiles, 1, 18 scum formation, 402, 404 silica, 28; opaline, 174;skeletal, 174 resilience (elasticity) of Scourfieldiales, 6 Table 1.1 siliceous cell walls, 25, 27, 53 communities to recover from sea bass (Morone), 428 silicification of diatoms, 13, 174 forcing, 304, 380, 383 sea birds, 428 silicon, 28; algal content of, 33 resistance of communities to sea combs (ctenophores), 263 Table 1.6, 173;cycling by diatoms, forcing, 304, 380 sea gooseberries (ctenophores), 253 174; deposition, in diatoms, 182, resource-based competition, 197, Table 6.1, 263 245; external SRSi concentrations 371 sea lamprey (Petromyzon marinus), half-saturating diatom growth, resource segregation, 205 290 197;relative to carbon, 174; respiration; basal rate, 108, 115, sea otters, 427 requirements of diatoms, 173, 132, 190; measurement of, 102; sea sawdust, 81, 166 197; silicon limitation of diatoms, ‘dark’ and ‘light’, 102, 189;asa sea urchin barrens, 426 196; silicon requirements of balance to excess photosynthesis, seals, 427, 428 Synurophyceae, 173; solution from 139, 239, 388 seasonality in phytoplankton sinking of diatoms, 174; sources, resting stages, 214, 249, 250 performances, 231, 232, 234 27, 173; uptake by diatoms, 173 restoration of lakes by seaweeds, 12 sinking behaviour, of phosphorus-load reduction, 409; Secchi disk, 116, 118 phytoplankton, 39, 49, 50, 52, by sediment removal,, 413; using secondary sewage treatment, 399 243;ofcolonial aggregates, 63;of clay minerals, 413; sensitivity of sediment deposition, 249 cylindrical shapes, 50, 62;of systems to treatment, 413 sediment diagenesis, 250 oblate spheroids, 50;ofprolate resuspension of sedimented sediment focusing, 250 spheroids, 50;inrelation to material, 79, 250 sediment semi-fluid surface layer, mixed-layer depth, 70 retention time (hydraulic), 240, 241 249 relevance to nutrient uptake, Reynolds number, of water flow, 45, sediment traps, 220, 246 147;ofsculpted models of algae, 50, 243;ofparticle motion, 49, 50 sedimentary flux, 284, 388, 390, 50, 51; spherical shapes, 50; rhizopods, 252 Table 6.1, 292 430;ofphytoplankton, 247, 249, of stellate colonies, 63 rhodophytes, 11, 12 318 534 GENERAL INDEX

sinking behaviour (cont.); of storage products of phytoplankton, trace elements, 167 teardrop shapes, 51; vital 6 Table 1.1, 7 Table 1.1, 25, 26 trait selection, 362 regulation of, 52, 65, 66, 123, 246 Table 1.2 trait-separated functional groups of sinking-rate determination, 51 stratification of the water column, freshwater phyoplankton, 319, size-efficiency hypothesis, 278 73, 75, 79, 204 320 Table 7.1, 346, 347 Table 7.6, size spectra of phytoplankton straw, anti-algal effects of, 405 394 assemblages, 348 structural viscosity, 67 Tribonematales, 6 Table 1.1 slime moulds, 295 structured granules, 25 tripton, definition of, 2 sodium, 28; algal requirement for, succession, in terrestrial plant trishydroxymethyl-aminomethane 172;cyanobacterial requirement communities, 204;inthe (tris), 168 for; , 172 plankton, 303, 359, 370, 384 trophic cascades, 263, 288 soil chemistry, 398 succession rate, 366 trophic states, 400; separation SOIREE oceanic iron fertilisation, successional climax, 304, 359, 365 criteria, 401 Table 8.1 170, 308 sulphate, algal requirement for, 172 tuna (Thunnus), 428 solar energy income, 41;asa sulphur, algal content of, 28, 32, 33 tunicates, 258 Table 6.1, 261, function of latitude, 41 Table 1.6 262 solar constant, 41, 95 sulphur-reducing bacteria, 5, 193 turbellarians, 253 Table 6.1 solar energy income, 108 supportive capacity, 346 turbulence, 42, 46;inconfined solar heat flux, 72 surface avoidance by flagellates, 83 channels, 46; associated with soluble reactive silicon (SRSi), 173 surface-area-to-volume ratio in moving particles, 49 species composition in marine phytoplankton, 185 turbulent dissipation, 47, 71;rate plankton, 302;inlimnetic surface mixed layer, 47, 204; of, 47, 48, 48 Table 2.2 plankton, 318;inrelation to light mixed-layer depth, 48 Table 2.2, turbulent embedding of deficiency, 345;inrelation to 71, 74, 75, 79, 80, 204, 244; mixed phytoplankton, 48, 49 nutrient deficiencies, 345 depth, in relation to light turbulent extent, 69 species richness of phytoplankton penetration, 117, 119, 138, 244; turbulent intensity, 74, 75 assemblages, 354, 364, 366, 367; relative to phytoplankton sinking turbulent kinetic energy, 47 a-, β-, ?-diversity, 380, 394; rates, 244;artificial enhancement turbulent velocity, 39, 45, 46, 48 relevance to community of, 414 Table 2.2, 69; fluctuations of, 45, functioning, 382;inrelation to suspension of planktic organisms, 1, 46 successional maturation, 384 17, 38 turgor pressure, 57, 59 species selection, in oligotrophic Synurales, 7 Table 1.1 tychoplankton, 1, 2 systems, 203;inrivers, 242 synurophycaens, 25 specific heat, of water, 16, 41 ‘Swimming’ velocities in ubiquity of phytoplankton, 353 spirotrichs, 252 Table 6.1, 259 phytoplankton, 49, 68, 83, 205 Ulotrichales, 6 Table 1.1, 12 squid (cephalopods), 256 Table 6.1, ‘Telescoping’ of algae at the surface, ultraplankton, 2, 4 264 402, 404 Ulvales, 12 stability in phytoplankton ultraviolet radiation, protection communities, 304, 381 tench (Tinca), 423 from, 123 standing crop, 223 terrestrial sources of POM, POC, 390 underwater light fields, 108, 110, starch, 6 Table 1.1, 7 Table 1.1, 25, Tetrasporales, 6 Table 1.1, 12 111, 119 98, 189 thalliaceans, 258 Table 6.1, 261, 262 upwellings, 308 statoblasts, 257 Table 6.1, 353 thermal bar, 89, 324 urea, as a source of nitrogen stoichiometric lake metabolism thermal stratification, 73, 75, 290 available to phytoplankton, 163 model, 401 thermocline, 74, 75 Utermohl¨ counting technique, 179 stoichiometric oxygen demand of thylakoids, 10, 12, 25, 96, 146; decomposition, 296 assembly, 168 vacuoles, 25 stoichiometry, as an ecological tides, 42 vanadium, 28, 167, 335, 398 driver, 199, 287 tidal mixing, 42, 48 Varzeas´ (flood-plain lakes), 352 Stokes’ Equation, 49, 51, 243 total iron (TFe), 169 vascular plants, 11 stolothrissids, 389 total phosphorus (TP), 155, 399 velocity adaptation of nutrient stoneworts, 419 toxic algae, 312, 401, 407 uptake, 157, 194, 202 storage adaptation of nutrient toxic metals, 167;redox sensitivity velocity gradients through water uptake, 157, 194, 202 of, 167 columns, 47, 80, 83 GENERAL INDEX 535

vertical migration of viscous behaviour of, 44, 49; young-of-the-year (YOY) fish, 289 phytoplankton, 205 specific heat of, 41 viruses, 2, 5, 292, 295 water, expansion coefficient of, 72 zeaxanthin–violoxanthin reaction, viscosity of water, 39 Table 2.1, 40 watermovements, 17, 38, 39, 41, 47, 123 vitamins, 170; microalgal benefits 77 zebra mussel (Dreissenia polymorpha), from, 170;B12 requirements of water blooms, 56, 81, 401 290, 323 phytoplankton, 170 Wedderburn number, 74, 75, 243 zeta potential, 67 Vollenweider–OECD model, 399, WETSTEM electron microscopy, 67 zinc, 28, 167 400, 408, 410 whales, 263, 428 zoobenthos, 392, 395 volume; of the ice caps, 39;of ‘white water’ events, 13 zoomastigophorans, 251, 252 Table inland waters, 39;ofthe sea, wind action, 42;stress applied to 6.1 39 water, 46, 69;velocity, 46 zooplankton, 2, 2, 251;phyletic Volvocales, 6 Table 1.1, 12, 25; DIC classification of, 252 Table 6.1;to, requirements of, 130 X-ray microanalysis, 167 258 Table 6.1; anti-predator vorticellids, 259 xanthophylls, 12, 13, 25, 95;, 115, defences, 269;growthrates of, 123 274; competitive interactions Water, physical properties of, 16, 39; Xanthophyta, 12, 25; classification among calanoids and cladocerans, et seq., 39 Table 2.1; molecular of, 6 Table 1.1 286; zooplankton and optimal structure, 39 foraging by fish, 392, 394 density of, 39 Table 2.1, 40; yellow perch (Percaflavescens), zoospores, 66 viscosity of, 39 Table 2.1, 40; 290 Zygnematales, 6 Table 1.1, 12