, STATUS AND ROLE OF

C. S. Reynolds Freshwater Biological Association and NERC Institute of Freshwater Ecology

I. The Structure of Planktonic Communities reproduce on organic carbon sources, taken in dis- II. Habitat Constraints in the Plankton solved or particle form. III. Form, Function, and Selection in the metazoan Literally, a multicelled animal. Phytoplankton mixotrophy The ability of a normally autotrophic or- IV. Form, Function, and Selection in the ganism to switch, circumstantially, to phagotrophy, Zooplankton or to support an otherwise meager food supply by V. Function in the Bacterioplankton resorting to the ingestion and assimilation of bacteria VI. Temporal Patterns in the Organization and or their products. Diversity of Planktonic Communities pelagic The (open-water) part of the aquatic environ- VII. Mechanisms Promoting and Maintaining ment that is far from the shore and the bottom bed. Diversity in the Plankton phagotrophy A type of heterotrophy that involves the VIII. Conclusions and Implications consumption of protists, plants, or animals as food. photoautotrophy A type of autotrophy in which organ- isms gather light energy in order to reduce carbon dioxide to organic carbon; characteristic of green GLOSSARY plants, most algae, and some prokaryotes. prokaryote Organizational state of cells lacking a mem- autotrophy The ability of organisms to grow and repro- brane-bound nucleus and certain other organelles. duce independently of external sources of organic Bacteria, including the Cyanobacteria, are typically carbon compounds. prokaryotic. Ͻ Ȑ An organizational state of cellular organisms picophytoplankton The smallest ( 2 m) size class in which the genome of the cell is stored in chromo- of photoautotrophic plankton. somes enclosed in a membrane-bound nucleus; all protists (algae and protozoa), fungi, plants, and ani- mals are . euphotic The top layer of a water body through which ‘‘PLANKTON’’ IS A COLLECTIVE TERM for organisms sufficient light penetrates to support net photosyn- adapted specifically for a life passed mainly in suspen- thetic gain and the growth of photosynthesizing or- sion in the open waters (the pelagic zone) of the sea ganisms. Rarely more than 100 m in depth, the eu- and of such inland waters as lakes, reservoirs, and rivers. photic layer can be as little as 1 m in turbid waters. Planktonic organisms include protists (allegedly sim- heterotrophy The ability of organisms to grow and ple, unicellular, or colony-forming algal primary pro-

Encyclopedia of Biodiversity, Volume 4 Copyright  2001 by Academic Press. All rights of reproduction in any form reserved. 569 570 PLANKTON, STATUS AND ROLE OF ducers and their protozoan consumers), microorgan- and its solvent properties, which maintain nutrients isms, and certain types of small metazoan animals, all and metabolic gases in readily assimilable state. sharing a common liability to passive entrainment in In truth, however, the planktonic ways of life have water currents, generated by tide, wind, convection, evolved to accommodate several problems and draw- gravity, and the rotation of the earth. The inherent backs associated with living in open water. Dominant physical variability of open-water habitats typically fa- among these is the issue of turbulence. Water molecules vors absolutely short life histories; rapid changes in experience strong mutual attraction, which makes the dominant composition, in response to fluctuat- liquid relatively viscous when compared to other fluids. ing environmental conditions, contribute to the mainte- Seeing waves break on the shore, or watching ‘‘white’’ nance of high biological diversity in individual habitats water plunging through riverine rapids, we may be casu- and to the survival of a high species richness among ally impressed by the fluidity of water flow but, without planktonic assemblages in general. the driving energy, calm is rapidly reestablished as vis- cosity overcomes the residual motion at the molecular level. What happens is that the introduced mechanical energy is dissipated through a cascade of propagating I. THE STRUCTURE OF eddies, of diminishing size and velocity, until molecular PLANKTONIC COMMUNITIES attraction imparts order over chaos and the molecular movement is overwhelmed. This behavior is now mea- The functional definition of plankton, ventured at the surable and it has been mathematically described (see, introduction to this chapter, has superseded the origi- for instance, Mann and Lazier, 1991). What is of partic- nal, nineteenth-century allusions to plankton ‘‘floating’’ ular interest here is that, depending upon the intensity in water. Nevertheless, even this is still unsatisfactory, of persistent wind- or gravitational forcing, viscosity for its implication that the suspension is either complete overcomes inertia within the range 0.2 to 3 mm (see or continuous is strictly erroneous. However, genuinely Reynolds, 1997b, for examples). This means that the planktonic organisms—which include the plantlike, immediate environment experienced by organisms chlorophyll-containing primary producers of the phyto- smaller than this (i.e., most of the phytoplankton, bac- plankton, the heterotrophic, decomposer microorgan- terioplankton, and the smaller components of the zoo- isms of the bacterioplankton, and the more animal-like plankton) is wholly viscous: far from being fluid, the consumers of the zooplankton—are too small (often forces acting on the microorganism are comparable to Ͻ20 mm) for their own intrinsic movements to be able those experienced by a human immersed in treacle or to overcome, often or at all, the dispersive effects of unset cement. The organisms do not experience turbu- water movement. Thus ‘‘embedded’’ within the tireless lence, neither are their delicate morphologies threat- and unconstrained motion of open water, planktonic ened with physical damage, but they remain entrained organisms broadly go wherever the flow takes them. In in the turbulent field and continue to be randomized this way, the ecology of plankton is inextricably related throughout its spatial extent. Larger zooplankton (say to the physical properties of the medium, the extent Ͼ0.2 mm), though still too feeble to resist entrainment and limits of its motion, and the environmental condi- consistently, are sufficiently tough and flexible to toler- tions set within these bounds (Reynolds, 1997b). This ate the millimeter range of turbulence and to exploit it situation contrasts with that of most fish and other effectively in food gathering (Rothschild and Os- larger (Ͼ20 mm) animals of open water—the ‘‘nek- borne, 1988). ton’’—whose swimming strength is usually able to over- Beyond the selective constraints imposed by the come normal movement of the water. physical properties of pelagic, open-water environ- The older literature also promulgated a view that ments, it is also necessary to recognize that, with respect suspension in water was necessarily beneficial, suppos- to the obligate material components of living cells, the ing water to be something of an ideal habitat. Living aqueous concentrations of some of these (especially in water does confer some notable positive advantages carbon, nitrogen, phosphorus, iron, and fifteen or so over terrestrial or aerial habitats. These include the micronutrient elements) are often so dilute that their mechanical (‘‘Archimedean’’) support water provides, availabilities place a severe constraint on the assembly as a consequence of its much greater density in compari- of planktonic biomass. Moreover, despite its alleged son with air; its slow temperature fluctuations, as a transparency, the absorbance of solar energy by pure consequence of its much higher specific heat than air; water (see, for instance, Kirk, 1994) is such that, at PLANKTON, STATUS AND ROLE OF 571 depths of Ͼ100 m, it is always as dark as night. Biologi- nia et al., 1991). The total number recorded from inland cal productivity in lakes is often severely constrained waters is not certainly known, but it is estimated that by rarefied resources or by deficiencies in processing there are quite 4000 of these as well (Reynolds, 1996). energy, or by both. Far from being an ideal environ- Few genera and still fewer species are common to both ment, the pelagic is a rather unpromising medium for fresh and salt waters. Even if a fairly conservative view successful exploitation by living communities. of their classification is adopted, the species are drawn Yet, within this general constraint, there is a remark- from at least six distinct protist phyla and at least two able richness of individual species inhabiting the plank- major prokaryote subdivisions (see Table I). The Purple ton of the world’s lakes and seas. Not all have even been (Chromatiaceae) and Green Sulfur Bacteria (Chlorobi- adequately described and separated. The extraordinary aceae) are represented in specialized, anoxic habitats. diversity and phyletic representation of planktonic or- Of the planktonic genera of Cyanoprokaryotes (for- ganisms may only be hinted at in the following subsec- merly classed as Cyanophyceae, or ‘‘blue green algae,’’ tions. As a preface to any such review of the planktonic and now most commonly referred to as ‘‘Cyanobacte- biota, however, it is necessary to emphasize that the ria’’) most occur in lakes, though several are also com- familiar separation, first of plants and animals and then mon in the low-salinity (Ͻ11 parts per thousand) areas their subdivision among phyletic divisions, cannot be of the Baltic. ‘‘Sea sawdust’’ (Trichodesmium spp.) is applied too rigidly. This is not simply a reluctance to found in low-latitude seas. The Cyanoprokaryotes are take sides with rival claimants about whether photosyn- also well represented among the smallest marine and thetic protozoa or bacterivorous algae are essentially freshwater primary producers (the picophytoplankton: plant or animal: most can be regarded as members of cells Ͻ2 Ȑm in diameter; Waterbury et al., 1979). an ill-defined of Protista, which comprises The more conspicuous components of the phyto- mainly unicellular eukaryotic organisms, including the plankton of the open sea belong to the Pyrrhophyta more plantlike photoautotrophs and the more animal- (including a wide variety of dinoflagellate species) or like phagotrophic consumers of other organisms or to the Chrysophytes. This large division is taken to their products. The convenience of distinguishing include the large number of species, drawn from planktonic ‘‘plants’’ and ‘‘animals’’ by function (Tables one or other of the two main orders (the centric Biddul- I and II) does not necessarily correspond to any funda- phiales and the pennate Bacillariales), as well as a diver- mental evolutionary or phyletic separation. Even the sity of elaborate, scale-bearing Coccolithophorids. names applied to the subdivisions follow past conven- Besides and Cyanoprokaryotes, the more tion rather than convey any emerging understanding of conspicuous components of the freshwater phytoplank- the molecular affinities of the various groups of protists. ton may be contributed from among the many chlo- The perplexity is yet greater when referring to the bacte- rophyte and chrysophyte orders. However, cryptomo- ria: whereas the lack of a membrane-bound nucleus nads, peridinians, chloromonads, and euglenoids can and of certain other intracellular organelles provides a all occur in large numbers at certain locations. robust separation of their prokaryotic organization from the cells of eukaryotes, it is still difficult to distinguish among most bacteria other than by their biochemical B. Marine Zooplankton activities and their affinities at the molecular level. Rela- The number of species of represented in the zooplank- tively ‘‘safe ground’’ is reached only among the more ton of the sea is considerably enriched by the distinctive distinctive metazoan phyla, though even there, affinities dispersal stages of many marine animals that spend among the main groups are often still obscure. their adult lives in the littoral or the benthos. To dif- fering extents, these larvae (the amphiblastulae of sponges, the medusae and ephyrae of the cnidarian A. Phytoplankton coelenterates, the pilidia of nemerteans, the trocho- Taking the capacity for photoautotrophy, the ability to spheres of polychaetes, the cypris larvae of cirripedes, manufacture organic carbon compounds through the the phyllosomae and zoeae of the eucarid malacostraca, photosynthetic reduction of carbon dioxide, to be the the veligers of the lamellibranch mollusks, the various sole distinguishing criterion for separating them from auriculariae, bipinnariae, and plutei of the echinoderms other planktonic organisms, the phytoplankton is still and the appendicularian larvae of the ascideans; see extremely diverse. More than 4000 species of marine Table II) share the diminutive size ranges, membranous phytoplankton have been named and described (Sour- translucence, and feeble swimming movements charac- TABLE I Phytoplankton in Freshwater and Marine Systems

Freshwater phytoplankton Marine phytoplankton Freshwater phytoplankton Marine phytoplankton

Prokaryota Class: Synurophyceae Division: Anoxyphotobacteria Order: Synurales Family: Chromatiaceae Synura, Mallomonas Thiopedia, Thiodictyon Class: Bacillariophyceae Family: Chlorobiaceae Order: Biddulphiales Chlorobium, Pelodictyon Urosolenia, Aulacoseira, Rhizosolenia, Cyclotella, Division: Cyanoprokaryota Cyclotella (‘‘blue-green algae’’) Stephanodiscus , Thalassiosira, Order: Chroococcales Skeletonema, Ethmodiscus Synechococcus, Microcystis Synechococcus Order: Bacillariales Order: Bacillariales Order: Nostocales , Synedra, Asterionella, Nitzschia Anabaena, Aphanizomenon Trichodesmium Cylindrospermopsis Class: Haptophyceae Gloeotrichia Order: Prymnesiales Order: Oscillatoriales Chrysochromulina, Chrysochromulina, Isochrysis, Planktothrix, Limnothrix, Prymnesium Phaeocystis Pseudanabaena, Lyngbya, Order: Coccolithophoridales Phormidium Emiliana, Florisphaera, Eukaryota Gephyrocapsa, Umbellospaera Phylum: Cryptophyta Class: Xanthophyceae Class: Cryptophyceae Order: Mischococcales Order: Cryptomonadales Monodus, Ophiocytium Cryptomonas, Chilomonas Cryptomonas Order: Tribonematales Rhodomonas Tribonema Phylum: Pyrrhophyta Phylum: Euglenophypta Class: Dinophyceae Class: Euglenophyceae Order: Peridiniales Order: Eugleninales Order: Eugleninales Peridinium, Ceratium, Peridinium, Ceratium, Euglena, Phacus, Eutreptia Ornithocerus, Trachelomonas Glenodinium Dinophysis, Scrippsiella, Phylum: Gymnodinium, alexandrium, Class: Prasinophyceae Gonyaulax, Gyrodinium Order: Pedinomonadales Class: Adinophyceae Pedinomonas Order: Prorocentrales Order: Halosphaerales Prorocentrum, Pyrocystis Halosphaera Phylum: Raphidophyta Class: Euchlorophyceae Class: Raphidophyceae Order: Volvocales Order: Chloromonadales Chlamydomonas, Dunaliella, Nannochloris Gonyostomum Volvox, Eudorina Phylum: Chrysophyta Order: Class: Chrysophyceae Gemellicystis Order: Bicosoecales Order: Chlorococcales Bicosoeca Chlorella, Ankyra, Order: Pediastrum, Chromulina, Ochromonas, Coelastrum, Dictyos- Dinobryon, phaerium, Chrysosphaerella, Uroglena Scenedesmus, Order: Hibberdiales Sphaerocystis Class: Order: Ulotrichales Order: Geminelle Pedinella Order: Zygnematales Order: Closterium, Stauatrum Distephanus, Dictyochoa

572 TABLE II Zooplankton in Marine and Freshwater Systems

Marine zooplankton Freshwater zooplankton Marine zooplankton Freshwater zooplankton

Phylum: Mastigophora Class: Branchiopoda Bodo, Peranema Order: Anostraca Phylum: Craspedomonadina Chirocephalus (Choanoflagellates) Order: Diplostraca Monosiga (Cladocera) Phylum: Rhizopoda Evadne, Podon Diaphanosoma, Ho- Order: Amoebina lopedium, Pelomyxa Bosmina, Daphnia, Order: Foraminifera Ceriodaphnia, Globigerina Arcella, Difflugia Monia, Simocephalus, Order: Radiolaria Bythotrephes Acanthometra Class: Ostracoda Order: Heliozoa Gigantocypris Cypria Actinophrys Class: Copepoda Order: Cyclopoidea Phylum: Ciliophora Oithona Mesocyclops Order: Holotricha Chondracanthus Ergasilus Colpoda Nassula, Colpoda Order: Calanoidea Order: Spirotricha Calanus, Temora, Eudiaptomus, Eurytemora, Euplotes, Caenomorpha, Centropages Boeckella Halteria, Class: Branchiura Metopus, Strombidium, Argulus Tintinnidium Class: Cirripedia Order: Peritricha [Cypris larvae] Vorticella, Epistylis Carchesium Class: Malacostraca Phylum: Porifera Order: Peracarida [amphiblastula larvae] (Suborder: Mysidacea) Phylum: Coelenterata Leptomysis Mysis Subphylum: Cnidaria (Suborder: Cumacea) Order: Leptomedusae Diastylis Obelia (Suborder: Isopoda) Order: Anthomedusae Eurydice Hydractinia (Suborder: Amphipoda) Order: Trachylina Apherusa Macrohectopus Limnocnida, Craspedacusta Order: Eucarida Order: Siphonophora (Suborder: Euphausiacea) Velella, Physalia Nyctiphanes, Euphausia Subclass: Scyphozoa Phylum: Arthropoda Aurelia, Cyanea, Pelagia Class: Insecta [all larvae] Subphylum: Ctenophora Order: Megaloptera Class: Tentaculata Sialis Pleurobranchia Order: Diptera Class: Nuda Pontomyia Chaoborus Beroe¨ Phylum: Mollusca Phylum: Platyhelminthes Class: Gastropoda Class: Turbellaria Order: Opisthobranchiata Convoluta, Microstomum Limacina, Clione Phylum: Nemertea Class: Lamellibranchiata [pilidium larvae of certain [Veliger larvae] Dreissenia [veliger] Hoplonemertines] Phylum: Nematoda Phylum: Chaetognatha [A few shelf-water Sagitta species are described] Phylum: Echinodermata Phylum: Rotatoria [larvae: plutei, auricu- Order: Monogonota laria, bipinnaria, etc.] (Suborder: Flosculariacea) Flinia, Conochilus Phylum: Chordata (Suborder: Ploima) Brachionus, Keratella, Subphylum: Tunicata Kellicottia, Class: Ascidiacea Synchaeta, Asplanchna [appenicularia larvae] Phylum: Gastrotricha Class: Larvacea [Encountered in plankton Oikopleura of small water bodies] Class: Thaliacea Phylum: Annelida Doliolum Class: Polychaeta Subphylum: Verterata Tomopteris Class: Actinopterygii [trochosphere larvae] [larval fish] Phylum: Crustacea

573 574 PLANKTON, STATUS AND ROLE OF teristic of the species which are planktonic throughout Clupeids (herrings, sardines) and Scombrids (Mack- their lives. Among the smallest (Ͻ20 Ȑm) examples erel) fulfill this description; ultimately demersal Gadids of these heterotrophic protists are the nanoflagellates (cods and allies) and benthic flat fish (Pleuronectids, (some being closely allied to the photoautotrophic phy- Soleids) also pass planktonic dispersal stages. toflagellates, classified here as phytoplankton) and cho- anoflagellates. The microzooplankton fraction (in the size range, 20–200 Ȑm) includes the rhizopod forami- C. Freshwater Zooplankton niferans and radiolarians, and a range of ciliate and The phyletic representation in the zooplankton of lakes suctorian ciliophorans. More conspicuous (0.2–20 is well known to be relatively much poorer than in the mm) in the marine zooplankton are the ctenophoran sea, but mostly this reflects the poorer representation ‘‘comb jellies’’ and sea-gooseberries, the chaetognath of the animal phyla among fresh waters anyway. The ‘‘arrow worms’’ (e.g., Sagitta), some specialized turbel- summary in Table II shows considerable coincidence larians (e.g., Convoluta, Microstomum) and polychaetes of representation at the higher phylogenetic levels but, (e.g., Tomopteris), certain opisthobranch gastropods as with phytoplankton, there is almost no commonality (such as Clione, Limacina), and the larvaceans (e.g., of species. Oikopleura) and salps (e.g., Doliolum). Protists usually figure prominently in the plankton The most prominent of the animals of the marine of inland waters, supposedly as a function of the organic plankton, however, are crustaceans. Most of the species matter available, including detrital particles and their are copepods, including calanoids, like Calanus, Tem- associated bacteria. The smaller heterotrophic flagel- ora, and Centropages, and cyclopoids, such as Oithona. lates generally consume free-living bacteria, but many There are also some representative cladoceran (e.g., of the common planktonic microciliates, like Coleps and Evadne, Podon) and ostracod (such as Gigantocypris) Tintinnidium, feed also on small algae and flagellates. In genera. The malacostracan orders are distinctively rep- doing so, they fulfill an important linkage in the so- resented by organisms that remain planktonic in their called microbial loop (Azam et al., 1983): in many sys- adult stages. Mysidaceans (such as Leptomysis) are lo- tems, the excretion of excess organic carbon fixed in cally abundant and a few cumaceans (e.g., Diastylis) , its assimilation by bacteria and its suc- are remarkable for being nocturnally planktonic and cessive transfer through closely coupled flagellate-cili- diurnally benthic in coastal waters. Amphipods (e.g., ate consortial linkages to copepod consumers and, even- Apherusa) and isopods (e.g., Eurydice) have planktonic tually, planktivorous fish, demonstrably exceeds the representatives. Perhaps the most renowned compo- carbon transfers along the conventional phytoplankton nent of the plankton of the high-latitude oceans, mainly Ǟ zooplankton Ǟ fish trophic pathway. for being one of the major food sources of the filter- Occasionally, the larger Amoebae and ciliates, such feeding whales, is krill (Euphausia spp.). Elsewhere, the as Nassula, may dominate the zooplankton; this may smaller euphausids form an important food for pelagic owe to the prevalence of a particular food source, or fish: Nyctiphanes is one of the common genera in Euro- to the fact that a crustacean plankton has not yet devel- pean coastal waters. oped, or that some other factor (low oxygen concentra- Some of the cnidarian jellyfish may be regarded as tion, for example) restrains potential competitors for being the largest animals in the plankton (Ͼ20 mm, the same food resource. perhaps to 2 m). Though some of these are rather larger At least two freshwater coelenterate genera have than some of the swimming organisms (‘‘nekton’’: fish, planktonic medusae. The Gastrotrich phylum of mi- cephalopods) that are excluded from the understanding nute, wormlike but unsegmented animals is occasion- of ‘‘plankton’’ (discussed earlier), the large jellyfish ally represented by planktonic specimens. The phyloge- qualify for their poor ability to control their own move- netically close phylum of the Rotatoria is prominently ments in the sea. The siphonophores, like Velella and represented in the freshwater plankton by some two the Portuguese man o’war, Physalis physalis, are little dozen genera, drawn mainly from the Order Monogo- more than drifting ‘‘polyp colonies.’’ The true jelly-fish, nonta. The most ecologically important genera include which move themselves by slow, rhythmic pulsation of Asplanchna, Brachionus, Filinia, Keratella, Kellicottia, the umbrella-like manubrium, include the distinctive and Synchaeta. Some colonial rotifers also feature in the Aurelia, Cyanea, and Pelagia. plankton (e.g., Conochilus). Some are specialist feeders; Finally, the young stages of several species of pelagic most of those mentioned browse or filter-feed on bacte- fish are of such diminutive size and swim so feebly and ria, detritus, and planktonic algae, generally within spe- with weakness of motility that, for the first part of their cies-specific size ranges (Pourriot, 1977). lives, they are reasonably included among the plankton: As in the sea, the most prominent planktonic animals PLANKTON, STATUS AND ROLE OF 575 are crustaceans. The Branchiopods are represented by and animal-species surveyed previously is counter- the anostracan ‘‘brine shrimps’’ (e.g., Chirocephalus), intuitive and paradoxical (Hutchinson, 1961). especially in temporary waters, and by the Cladocera, Neither is it clear for how long such richness has the familiar ‘‘water fleas.’’ This grouping (its monophy- distinguished the biota of open waters. Owing to the letic origin is now doubted) includes the mainly herbiv- facts that most microorganisms do not form robust orous, filter-feeding species of Daphnia, Ceriodaphnia, fossils, that given freshwater habitats are, in geological Moina, Simocephalus, Bosmina, and Holopedium, and the terms, very transient features, and that, at the relevant predatory Bythotrephes and Leptodora. Planktonic Os- evolutionary scales, even the present ocean floors are tracods are noted from lakes in Southeast Asia (Cypria relatively young, it is difficult to be categorical about javensis) and from Laguna de Pete´n, Guatemala (Cypria the origins of planktonic communities. However, they petenensis). The Copepods are particularly well repre- are likely to be old. By the beginning of the Cambrian sented by calanoids (such as Eudiaptomus, Eurytemora, period, some 600 million years before present, when Boeckella) and by Cyclopoids (e.g., Mesocyclops); some some of the oldest fossiliferous sedimentary rocks were parasitic Cyclopoids (e.g., Ergasilus) are dispersed formed, most of the invertebrate phyla represented in through the plankton. The Branchiurans (e.g., Argulus), modern plankton had already appeared. These were which are ectoparasitic on open-water fish, are certainly wholly aquatic, though not necessarily planktonic. The to be considered essentially planktonic. Though princi- Cyanobacteria had been established long before this, pally marine, the mysids are represented in the plankton with primitive oxygenic photosynthesis coccoid species of several high-latitude lake systems, where Mysis is already converting the reducing conditions of the early regarded as a relict from the last glaciation. The Amphi- planetary environment to an oxic one, between 2 and pod flag is carried by Macrohectopus, which is endemic 2.5 billion years ago. Many of the Protistan groups, to the plankton of Baykal Lake. including several of the eukaryotic algae, had also ap- Among the arthropod insects, several genera of Dip- peared by the Cambrian (Ragan and Chapman, 1978). tera have larvae, which pass most of their time in the Presumably, some of these were free living, in suspen- plankton. The most specialized of these are the juvenile sion in the water. The step to a truly planktonic exis- chaoborines (e.g., Chaoborus) or phantom midges, tence is supposed to be short and, with such a diverse whose transparent bodies reveal the internal provision phylogeny of modern plankton, it is reasonable deduc- of buoyancy-providing air sacs. The dispersal stages of tion that it was taken within each evolving group, per- aquatic larvae of other orders of insects sometimes show haps several times. It is probable that the first planktonic adaptations that are unmistakably planktonic: a striking communities began to come into existence about a bil- instance is provided by the first instars of Sialis (Mega- lion years ago, when many new opportunities for func- loptera; see Elliott, 1996). tional specialisms and the adaptive radiation of species were available. Interestingly, the various Chrysophyte groups are considerably younger, there being no undoubted re- D. Explaining Species Diversity cords from before the Mesozoic period (Tappan, 1980). The foregoing passages confirm the richness of phyletic Both the diatoms and the chromulines expanded and representation and the very large number of individual diverged during the Cretaceous era (135–65 million species that collectively contribute to the overall diver- years ago); the coccolithophorid Haptophyceae also ap- sity of planktonic organisms. The challenge now is to pear to have originated during the Mesozoic; it is their account for the richness of the planktonic species and biomineralized remains which predominate the chalk to explain the mechanisms by which it is maintained. deposits that have lent their name to the Cretaceous. At one level, we might be surprised that this problem Some very significant changes in the chemical com- arises at all. It should not be at all unreasonable to position of the sea must have occurred during that anticipate that, in a supposedly fluid and isotropic me- period. dium, fully accessible to suitably adapted species, Dar- While the same species may not have held sway winian selection should move the structure of the or- throughout, or even for the past 100 million years, ganismic assemblage toward just a small number of it is clear that the factors favoring a high planktonic specialists, each being the best-fit survivor in its key biodiversity are recurrent, if not ongoing. Many theories community role. Every less-fit competitor might be sup- have been advanced to explain Hutchinson’s (1961) posed to suffer progressive exclusion by the stronger paradox of the plankton, but the conundrum for long species; overall, diversity should be suppressed. Thus, remained unsolved. Either the number of occupiable to confront the remarkable richness of planktonic plant- niches must be far more numerous than had been sup- 576 PLANKTON, STATUS AND ROLE OF posed or the competition was somehow incomplete in rate sites of suitable habitat. It often takes anthropo- its effects. genic intervention to bridge these gaps, as the recent Hutchinson himself suspected that the assumption ‘‘breakout’’ of the lamellibranch, Dreissena polymorpha, of a homogeneous environment with steady-state prop- and hitherto endemic mysids from their original Cas- erties was flawed. Collectively, the environments that pian-basin locations into the waterways of Europe and, planktonic populations inhabit are subject to huge vari- now, North America graphically reminds us. Equally ability in their chemical makeup and in their physical remarkable is the arrival of the first freshwater Cladoc- characters. They may be physically separated from each era on Easter Island in 1780, which had failed to bridge other (as are freshwater catchments), enjoying quite the distance from the next nearest lake (over 3000 km different climates or, even if contiguous (like the seas), distant) prior to Captain James Cook’s requirement to their systems may be close to mutual isolation by cur- replenish his ship’s supply of drinking water (Du- rents and circulations. On the continents, lake basins mont, 1999). are created and destroyed at, relative to evolutionary The same student of plankton will also be well at- rates, high frequency. The skeletal understanding of the tuned to the seasonality of the species composition of history of the world’s oceans is that they have under- samples, as dominance moves frequently among the gone large oscillations in metabolism and productivity species of the assemblage. The differential responses of associated with changes in the biospheric carbon cycles individual species of plankton to temperature or day (Thierstein, 1989). Within the limits of habitat suitabil- length or nutrient resources are generally recognized ity that evolutionary specialization allows, the potential to underpin what is perhaps the most familiar feature ranges of individual species should be distinct from of planktonic communitie—the so-called seasonal suc- those that have evolved separate specialisms. Superim- cession. As with other aspects of plankton ecology, posed on the longer-term changes are relatively higher the identity of its driving variables has been actively frequencies of periodic forcing. Within these smaller pursued and described by conceptual word models; the habitat units, the higher frequency environmental oscil- most compelling of these has been the PEG-model of lations might lead to alternations in the favored special- Sommer et al. (1986). Like its less successful contempo- isms and consequent interspecific transfers of competi- raries, it is nevertheless founded on an implicit accep- tive advantage. Physical limitation of range (endemism) tance of the differences among planktonic species and or otherwise (cosmopolitanism) would then represent the suitability of species-specific adaptations to particu- the two extremes of dispersal efficiency across physical lar habitat constraints. barriers and habitat preferences. The successful pursuit of viable explanations for the Current understanding of plankton ecology con- origins of biodiversity and the mechanisms of its main- forms to this general view in that it is certainly possible tenance must acknowledge a distinction between ‘‘local for the experienced observer to determine the broad diversity,’’ a measurable property of the temporal com- habitat provenance of given planktonic assemblages: positional fluctuations in response to local, within- their species composition has an indicative value be- patch variability, and the total species richness, or over- cause similar assemblages characterize similar pieces of all biological diversity, which is supported by the aggre- water. Students of the plankton have usually accepted gate of patches and its continued ability to offer an a prevailing view that planktonic species are generally adequate number of accessible habitats to satisfy the cosmopolitan and disperse freely, so that, on balance, dynamics of survival of each species. The way to explain most are able to establish quickly wherever suitable planktonic biodiversity is through a simultaneous rec- conditions arise. Dispersal mechanisms among the pro- ognition of the variables constraining habitat suitability tists and prokaryotes are certainly effective (review of and the adaptive specialisms and limitations of species Kristiansen, 1996), and it is true that many convention- for which the habitat constraints will select and those ally identified morphotypes enjoy worldwide distribu- against which they will discriminate. tions. As more molecular information becomes avail- able, the cosmopolitan nature of plankton is called increasingly into question. Besides, the notion that ‘‘ev- erything is everywhere’’ is surely a matter of degree: II. HABITAT CONSTRAINTS ease and frequency of dispersal is not equal among IN THE PLANKTON planktonic species. Isolation and regional endemism certainly occur (Tyler, 1996), especially where long The assumption of a uniform, hospitable, steady state physical distances or significant, hostile barriers sepa- is erroneous so far as most open-water habitats are PLANKTON, STATUS AND ROLE OF 577 concerned. On the contrary, many are as hostile as their mal stability and down mixing in the tropics (for desert-like barrenness conveys. Relative infertility may examples, see Talling and Lemoalle, 1998). be locally or regionally attributable to an inadequacy So it is that the different kinds of water body (lake of light energy to sustain planktonic primary produc- or pond, river, estuary, coastal shelf, upwelling, or the tion and the import of organic carbon is too modest to open oceans) each offer, to the most appropriately support the heterotrophs. Light income may be scarce adapted species, or to those simply furnishing the for reasons of latitude (short day length, low solar decli- largest inocula, varied and sometimes very transient nation), or it may be severely ‘‘diluted’’ over a deep opportunities to build their local populations. Further- mixed layer, or its penetration may be abruptly curtailed more, because the medium is fluid and the movement by a high concentration of inert particles (turbidity). induced by wind or gravity is subject to fluctuations in Commonly, the concentrations of assimilable sources strength, the persistence and vertical extent of an upper, of certain primary nutrients place a very low ceiling on differentiated layer is a highly variable character of the the biomass that can be assembled (nitrogen, phospho- environment, which alters not just from season to sea- rus, and iron are cited most frequently as capacity- son but from day to day and from hour to hour. Interest limiting factors). Chronic nutrient deficiency also inter- is also growing in the effect of year-to-year variations. feres with the production of microbial biomass, even At all these scales, the intensity and frequency of the supposing there to be an adequate flux of organic car- environmental variability determine and, potentially, bon. For the planktonic animals, the problem is to be modify the critical habitat constraint and, hence, the able to forage sufficient food; the concentrations and the attributes of organisms most likely to benefit dy- size distributions of potential food particles influence namic performance. profoundly the nature and abundance of the consumer It follows that selective advantage is likely to move populations. A dearth of primary-producer plant bio- among species. Environmental variability is a powerful mass is no basis for the intense production of zooplank- influence on the assembly of planktonic communities ton, neither will it underpin large harvestable crops of and thus on their biological diversity. The causal link- prime pelagic fish. What we find is that the locations ages between observable patterns and processes in the where significant net primary production is possible maintenance of species diversity in the plankton may and that the occasions when it is exploitable by hetero- be usefully explored through a diagrammatic represen- trophic consumption are, in fact, strongly circum- tation of the two principal variables characterizing par- scribed. ticular open-water environments, namely, the fluctuat- Besides the spatial differentiation of planktonic ing fluidity or vertical extent of the uppermost water habitats, there is usually a considerable temporal layer and the availability of the resources to support variability. Conspicuous are the seasonal changes con- the assembly of biomass. The layout of Fig. 1 is de- sequent on latitude: lengthening spring days and scended from Margalef’s (1978) original scheme for higher flux densities are generic to all temperate marine phytoplankton, in which a ‘‘nutrient’’ axis is set ecosystems but for small organisms with short life against one of ‘‘turbulence’’; the arrangement is amena- spans, the changes are perceived by successive genera- ble to tracking habitat variability and the changing spe- tions and not as some perennial amplitude of fluctua- cies composition through time. The scheme has been tion registered by a forest tree, for example. Ambient developed for fresh waters to accommodate habitat con- temperature may increase too, incidentally raising the ditions in which nutrient resources and the light avail- threshold of wind energy required to keep the water ability in the surface-mixed layer are sufficient to satu- fully mixed. The onset of thermal stratification, as a rate the fastest in situ algal growth rates (in the top consequence of a shifting balance between the buoy- left corner of Fig. 1) and to distinguish them from ancy forces brought through surface warming and conditions that become either increasingly resource- the kinetic dissipation of the work of the wind energy, constrained (moving downward in the matrix), or in- precipitates a train of environmental effects, leading creasingly energy-deprived (moving rightward), or fall to enhancement of the segregation of the warm, deficient in both (bottom right corner). The selection insolated, aerated, and increasingly resource-depleted of given species or groups of species was found broadly epilimnion from a colder, darker, and potentially less to be correlated with the matrix space thus represented; oxidizing hypolimnion. Neither is such seasonality high-performance, fast-growing algae would be favored confined to high latitudes: even quite small differences in the relative paradise of the upper left-hand corner; in wind prevalence, cloud cover, humidity, and hy- algae favored by the second and third contingencies draulic exchange result in seasonal variations in ther- show some specialist adaptations, respectively, for op- 578 PLANKTON, STATUS AND ROLE OF

FIGURE 1 Two-dimensional representation of limnetic habitats, which, starting in the top left, distinguishes well- insolated, resource-replete water masses from (working down) long-stratified, resource-segregated water columns and from (working across) increasingly light-deficient environments. erating under conditions of low concentrations and re- sites that are chronically deficient in nutrients (points mote sources of nutrients, or for harvesting light from plotted well down the K** axis) from, on the one hand, low irradiances or from infrequent short periods in the those in which steep gradients develop as a consequence light field. The fourth, low-nutrient, low-light contin- of near-surface uptake (points track from high to low gency is unfilled and is something of a phycological on the K** axis) and, on the other, those in which the desert, evidently untenable as a habitat for a photoauto- nutrient is scarcely exhausted (points located consis- troph (Reynolds, 1988b). tently toward the top of the K** axis). It was never imagined that such a two-dimensional Against these axes, it is possible to characterize the matrix could describe the entire spectrum of freshwa- ‘‘signatures’’ of seasonal changes in various kinds of ter variability, but it has proved to be a consistent water body, including of small, ‘‘eutrophic’’ lakes, in template for predicting the structural responses of which nutrient availability is seasonally reduced, of planktonic assemblages to the main dimensions of shallow, fertile systems, in which the turbidity is the environmental variability. Latterly, effort has been predominant variable, and of deeper, oligotrophic sys- invested to improve both the utility and the quantifi- tems, where the depth of mixing is the strongest sea- cation of the axes. The horizontal axis in Fig. 1 sonal variable. An analogous (and in many ways, a more describes the integral, I**, which, as the product of self-evident) approach has been developed recently for the physical depth of mixing and the vertical attenua- the sea (Fig. 2). This distinguishes energy-limited, well- tion of a finite input of light energy, is sensitive to mixed, high-latitude oceans from the highly stratified, the constraints both of deep mixing and of high nutrient-segregated waters of the tropics and will repre- turbidity; quantities diminish rightward on a logarith- sent processes and interactions in coastal and shelf wa- mic scale. The vertical axis in Fig. 1 accommodates ters, including frontal zones and major upwellings of another composite scale, K**, being the quotient of the deep circulation currents. concentration of the critical nutrient in the medium The premise to be developed is that the biodiversity (usually the surface mixed layer) and the gradient of of plankton may be fitted to such templates and, more- concentration between the top and bottom of the over, that environmental change and variability select entire trophogenic layer. This scheme differentiates for alternative species. Reverberations in the selection PLANKTON, STATUS AND ROLE OF 579

FIGURE 2 Two-dimensional representation of some marine habitats, which separates the mixed (light deficient) and well-stratified (nutrient-segregated) from shallow, nutrient-rich shelf waters, as well as upwellings and frontal zones. As in Figure 1, moving away from the top left corner, habitats become increasingly resource-stressed (working down) or processing-limited (working across). Toward the bottom right (beyond the diagonal), habitats are ultimately untenable to photosynthetic autotrophs.

of the consumers and structural variance spread bon and adequate supplies of each of a score of other through the whole planktonic community. elements. Problems over the adequacy of the water sup- ply to phytoplankton may be safely discounted (water relations can be adversely affected by salinity changes, III. FORM, FUNCTION, AND where these result in the loss of cell water to the medium SELECTION IN THE PHYTOPLANKTON by osmosis). The main macronutrients (C, H, N, O, P, S, Na, K, Mg) involved in the synthesis of proteins, of A. The Basic Adaptations of cell protoplasm, and of the various organelles (all of which have to be replicated at each cell division), the Planktonic Photoautotrophs key micronutrients (Fe, Mn, Mo, Cu, Zn, B, Va) mediat- The essential environmental requirements of plank- ing the assembly processes, and the elements (Ca, Si) tonic photoautotrophs, to be able to grow in numbers condensed in the elaboration of calcareous and siliceous and increase in total biomass and to be able to perpetu- skeletal biominerals must be drawn into the cell from ate and disperse their genes, do not differ fundamentally the bathing medium, mostly against significant concen- from those of plants in other ecosystems: access to tration gradients. Elemental carbon, which constitutes water, exposure to adequate levels of photosynthetically nearly 50% of the dry mass of protoplasm, is usually active wavelengths of light, a source of assimilable car- distinguished as a separate resource to terrestrial plants 580 PLANKTON, STATUS AND ROLE OF because of the atmospheric source of carbon dioxide; variable. To operate habitually at more rarefied light for phytoplankton, the proximal source of carbon diox- levels clearly requires the provision of more, or more ide is that which is dissolved in the water and which, efficient, light-harvesting capacity. Moreover, because once again, has to be drawn into the cell against a steep it is frequently the case that the depth of the wind-mixed concentration gradient, itself sometimes exacerbated by layer extends beyond the euphotic layer, convective high organismic demand. So it is, in the dilute world entrainment of phytoplankton often diminishes its ag- of the plankton, that diffusion alone is rarely able to gregate exposure to the light field, at times leaving cells supply the resource requirements of plankton. Adaptive unable even to compensate their basic metabolic energy mechanisms for gathering chronically deficient re- requirement. Here, too, great adaptive importance at- sources include the enhancement of uptake affinity and taches to the sufficiency of the biomass-specific light- of the maximization of storage. Mechanisms enhancing harvesting provision and its presentation to the light access to remote reserves or for exploiting alternative field. At the same time, the planktonic photoautotroph sources of nutrients are valuable against a depleting still needs a suite of biochemical and physiological de- resource base. fenses to deal with the risk of overexposure of enhanced The biochemistry of the assembly processes is not light-harvesting that the extreme variability that pelagic the primary concern of the student of biodiversity, but it open water habitats present. is important to understand the essence of the metabolic machinery. Every activity, from resource uptake, through internal transport, protein synthesis, organelle B. Specializations among assembly, and operation, to the replication of new cells, requires the controlled expenditure of energy, which, Planktonic Photoautotrophs as in just about all living things, is supplied by the Because the fundamental requirements of (allegedly) respirational oxidation of carbohydrates. Fulfilling this simple plants are more readily measurable than are basal metabolic requirement constitutes an energetic those of more complex terrestrial ones, it is possible to maintenance cost to the organism. In the case of the quantify some of the generalized assertions about the heterotroph, additional energy is consumed in the for- selective value of species-specific adaptations to meet aging of foods—the essential requirement is that the the stress of deficiencies in the supply of resources investment of energy yields a greater return of potential and the processing constraints set by operating in a energy in the organic carbon thus derived. The distin- fluctuating environment. Starting with the quantum guishing feature of the photoautotroph is the ability to yield of photosynthesis, the theoretical output of 1 mol first generate the carbohydrate through the photosyn- of reduced carbon for the investment of 8 mol photons thetic reduction of carbon dioxide. The key reaction of photosynthetically active radiation harvested—or is the stripping of reductant (electrons) from water 0.125 mol C (mol photon PAR)Ϫ1—is demonstrably molecules. The energy to do this comes in sunlight approached in experiments with phytoplankton; typical (pretty well, the visible wavelengths) harvested in the measurements are 0.07–0.09 mol C (mol photon chlorophyll-protein complexes of the photosynthetic PAR)Ϫ1; (Bannister and Weidemann, 1984). Over the apparatus. Again, the functional architecture of the ap- temperature range, 10–30ЊC, and at the order of light paratus is not of primary concern here, but we should intensities required to saturate chlorophyll-specific recognize that what constitutes an adequacy of expo- photosynthesis in phytoplankton (50–200 mol photon sure to photosynthetically active light depends partly PAR mϪ2 sϪ1), photosynthetic yields are found to fall in on the efficiency of its interception and photochemical the range, 2–15 g C (g chlorophyll)Ϫ1 hϪ1. The carbon- conversion to carbohydrate and partly on the fraction fixation rate provides the capacity for assembling new of photosynthate that is required to satisfy the basal producer biomass. Taking an average 50 : 1 carbon-to- metabolic costs of its operation. chlorophyll ratio, exponential cell-specific growth ca- These criteria assume considerable ecological rele- pacities of 0.04 to 0.26 hϪ1 may be deduced, which vance to phytoplankton where, because of the sharp potentially might support biomass doublings from one underwater attenuation of downwelling sunlight, only every 17 h to one every 3 h. The maximum cell replica- the near-surface layer is readily supportive of net pri- tion rates in laboratory measurements on the unicellular mary production. Even then, seasonal, diurnal, and chlorophyte, Chlorella, one of the fastest-growing fresh- weather-determined fluctuations in the intensity and water eukaryotes, are equivalent to biomass doublings duration of incident sunshine means that the spatial every 19–4 h over the same temperature range (see and temporal extent of this euphotic layer is highly Reynolds, 1997b), comfortably within the theoretical PLANKTON, STATUS AND ROLE OF 581 carbon assimilation capacity. The shortfall is mainly streams) helps to offset the effects of capacity limitation attributable to consumption of fixed carbon during by carbon. growth (respiration). The distribution of metabolic limitations can be fit- For such rates of cell replication to be realized and ted to the I**-vs-K** ordination of planktonic habitats sustained, not only must the light levels and the carbon (Figs. 1 and 2). In the energy- and resource-replete dioxide supply be upheld, but all the other chemical environments represented toward their upper left cor- components resources have to be available in concentra- ners, the selective advantage resides with species tions that will also saturate the uptake demand. For adapted to the maximization of the opportunities for instance, the widely accepted stoichiometry of Redfield rapid resource exploitation and conversion to new bio- (1958) leads us to suppose that for every 42 mg C mass. Away from these areas, specialisms permitting incorporated, the new generation would, ideally, also continued operation under markedly subideal condi- require roughly 1 g P and 7 g N if the normal cell tions are selected. In the downward direction, the most stoichiometry was to be preserved. Taking the amount useful of these provide an advantageous measure of of new carbon dioxide that could migrate across the tolerance of resource stress—including the abilities to water surface to balance the consumption by primary conserve nutrient resources, to search for them more producers (about 100gCmϪ2 yϪ1; higher areal produc- efficiently, and to tap into other sources of resource. tivities in lakes and coastal waters are reliant on imports In the rightward direction, the derivation of harvestable dissolved in inflows and the reuse of respiratory carbon energy is progressively more interrupted and truncated: dioxide), the potential new production also requires adaptations for dealing with the disturbance to the pro- the supply of some 2.4 g P and 14 g N mϪ2 yϪ1. Moreover, cessing ability—including the enhanced ability to cap- the minimum direct PAR investment in biomass assem- ture photons from poor or fluctuating light fields—are bly would be not less than 100 mol photons mϪ2 yϪ1 increasingly demanded. (equivalent to a mean underwater photon flux of 10–20 It is possible to show consistent morphological and Ȑmol photon mϪ2 sϪ1: Reynolds, 1997b). adaptive traits among phytoplankton species that are Such theoretical calculations of the stoichiometric variously exploitative, disturbance tolerant, and stress capacities provided by the fluxes of each main resource tolerant. It is also possible to quantify the impacts of are helpful to the identification of which of them is adaptation and to demonstrate the satisfying coherence most likely to set the constraint on growth generally among the form, function, and ecology of planktonic and, hence, that to variations in which will evoke the algae (Reynolds, 1988b, 1995). For example, the species most sensitive changes in growth rate and supportable that appear in ‘‘new water bodies’’ (from rain puddles biomass. In this way, the factor group most likely to to tidal pools), in hydraulically (flood plain lakes after limit maximal attainment is revealed. In many kinds the river drops back) or seasonally refreshed systems of lake and seas, the total annual area-specific loads (lakes at the onset of thermal stratification) are typically (including recycled nutrient) of either nitrogen or phos- exploitatitive: they are characterized by ready and effec- phorus or both fall far short of the respective hypothe- tive dispersal mechanisms and by a facility for rapid sized saturation requirements of 14 g N and 2.4 g P growth (Ͼ10 ϫ 10Ϫ6 sϪ1 at 20ЊC). Typical freshwater mϪ2. So indeed the typically much lower standing crops representatives include such algae as Chlorella, Ankyra, of planktonic biomass are constrained by the rates of Koliella, Chlamydomonas, Rhodomonas, Chrysochromu- supply and reuse of critical nutrients. On the other lina, Monochrysis, Monodus, and Synechococcus. They hand, even in very clear water and under blue skies for are unicellular or form small coenobia (generally Ͻ103 12 h per day, the depth of the surface mixed layer and Ȑm3), offering a surface/volume ratio (Ͼ0.5 ȐmϪ1) its impact on the insolation of fully entrained algae favorable to rapid solute exchange and nutrient assimi- continue to impose a severe capacity limitation on lation. The area (e.g., of light field) projected by the planktonic primary production (Reynolds, 1997b: Fig. algal cell mass, usually a mark of its potential efficiency 45). Cold, oligotrophic seas and lakes are not exclu- as a light-gathering antenna, is equivalent to at least sively nutrient limited. However, it is where nutrients 6.5 m2 (mol cell C)Ϫ1. Reynolds (1995) proposed that are abundant, or are rapidly cycled in a shallow mixed these traits were indicative of an ‘‘invasive’’ or, in the layer, that we expect to see a level of phytoplankton terminology of Grime (1979), C-type life-history sufficient to challenge the carbon invasion rates, with strategy. an attendant rise in pH. In small lakes, internal recycling The adaptations that help species to survive devel- (carbon dioxide from community respiration, plus the oping nutrient stress include the physiological flexibil- carbon dioxide supplied in solution in inflowing ity to overcome deficiencies in the supply of carbon 582 PLANKTON, STATUS AND ROLE OF

(such as the ingestion of bacteria by the facutatively Not all phytoplankton species fit perfectly within phagotrophic dinoflagellates and chromulines), nitro- one or other of the three categories but show properties gen (‘‘fixing’’ the gas dissolved in the water, as occurs intermediate between them. What is interesting, how- in the facultatively produced heterocysts of Nostocalean ever, is that the intermediacy in morphological and Cyanobacteria), and phosphorus (producing phospha- physiological adaptation matches well the intermediacy tases to break the chemical bonds immobilizing ortho- in their ecologies. The ‘‘space’’ between the invasive and phophate in various particulate complexes). The ability the stress-tolerant acquisitive species is occupied by to conserve assembled biomass through reduction in genera such as Dinobryon, Dictyosphaerium, Sphaero- sedimentary and grazing losses is contributed by com- cystis, Gemellicystis, arguably Volvox, Eudorina, Aphani- bining motility (usually swimming) with large size: ease zomenon, and Gloeotrichia, which diminish in surface- of disentrainment and self-regulated migratory ranges area/volume ratio and maximum growth rate but give access to resources in the remoter parts of the increase in their abilities to exploit and conserve nutri- water column that may be denied to smaller species. ent resources. Freshwater algae between the invasive Freshwater examples (which include larger species of and the attuning poles include species of Cyclotella, Peridinium, Ceratium, Microcystis, and other colonial, Scenedesmus, and Coelastrum, which could be said to be bloom-forming Cyanobacteria and, arguably, such col- increasingly large, more convoluted, and increasingly ony-forming algae as Uroglena) are characteristically disturbance turbidity-tolerant algae. The axis between ‘‘large,’’ having cells or coenobia that are Ͼ104 Ȑm3 in stress- and disturbance-tolerance is occupied by rela- volume and often much more than 30 Ȑm in diameter). tively large, acquisitive, but self-regulating species, Their consequent rather low surface/volume ratios which can persist for months to years on stable density (Ͻ0.2 ȐmϪ1) leave the algae with slow rates of growth gradients, notably Planktothrix rubescens, P. mougeotii, (Ͻ8 ϫ 10Ϫ6 sϪ1 at 20ЊC), sensitivity to low tempera- and species of Lyngbya and Phormidium. Cryptomonas tures, and poor antennal projection (Յ2.5 m2 (mol cell shows traits almost intermediate between all three C)Ϫ1 ). The occurrence of growing populations of these extremes. stress-tolerant—S-type, or (‘‘acquisitive’’; Reynolds, 1995)—strategists tends to be restricted mainly to warm, well-insolated shallow lakes and epilimnia. C. Seasonality of Planktonic Autotrophs The phytoplankton species tolerant of, if not depen- The utility of the functional classification is best demon- dent on, near-continuous entrainment within deep or strated in relation to the complex issue of seasonal turbid mixed layers have well-developed capabilities for change. Despite its celebrated species richness, the phy- maintaining growth despite intermittent brief exposure toplankton is usually dominated by very few genera at to light. ‘‘Attuning’’ (Reynolds, 1995) strategists tolerate a time (it has been suggested that 95% of the extant this scale of pelagic disturbance through the projection standing biomass will be incorporated in no more than of a large mass-specific surface area (Ͼ8m2 (mol cell eight species at any one time; often it will be in rather C)Ϫ1 in the case of 1-mm threads of Planktothrix agard- fewer, as few as one or two; Reynolds, 1997b). Yet it hii; ȁ30 m2 (mol cell C)Ϫ1 in the case of an 8-celled is well recognized that the dominance moves among colony of Asterionella formosa). They have high surface- different species through time and that, in a given sys- to-volume ratios (generally Ͼ0.5 ȐmϪ1) though these tem, the sequence will be similar from one calendar are not necessarily attained through small unit-size but year to the next. Moreover, similar patterns may be by morphological complexity (filaments, attenuated or observed in similar but often geographically remote fenestrated coenobia, protuberances, etc.) and so con- lakes. Numerous such cycles have been described in tinue to benefit from reasonably rapid rates of cell- the literature (Reynolds, 1984b; Sommer et al., 1986); specific nutrient uptake and growth (Ͼ10 ϫ 10Ϫ6 sϪ1 it is sufficient to mention a single archetypal example. at 20ЊC). The potential for energy conversion may be In a small, calcareous, temperate lake in Britain (Crose enhanced by an increased cell-specific chlorophyll con- Mere), the diatom Asterionella dominates the early tent and accessory pigmentation to widen the spectrum spring growth, increasing from a few tens to several of harvestable wavelengths. Other typical R species in- thousand cells per milliliter, over a period of six to eight clude larger diatom (e.g., Aulacoseira, Synedra), desmid weeks of lengthening days and intensifying insolation. (e.g., Closterium, Staurastrum), and Chlorococcalean Then, in mid-April, when the work of the wind is no genera (e.g., Pediastrum) and solitary, filamentous longer sufficient to discharge the increasing buoyancy members of the Oscillatoriales (like Limnothrix and of the heat flux to the surface, the lake will become Pseudanabaena). thermally stratified. Asterionella settles out of a mixed PLANKTON, STATUS AND ROLE OF 583 depth, which is too truncated to keep it in suspension, No two years will be exactly the same, and the rela- leaving the clear water open to the establishment of tive proportions of simultaneously dominant and co- such algae as Rhodomonas and Monodus, Cryptomonas, dominat species will fluctuate. Yet the pattern is robust and of the motile colonies of Eudorina. As the summer and is it amenable to diagrammatic summary (Fig. 3A): solstice approaches, these too are replaced, first by ni- against axes empiricized in terms of I** and K**, or trogen-fixing Aphanizomenon or Anabaena and by the even analogized to mixed depth versus the biologically dinoflagellate, Ceratium, which will dominate the an- available concentration of the critical nutrient, the time nual biomass maximum. In the autumn, the shortening trajectory of the changing coordinates traces the extent days and declining temperature lead to a weakening of of the seasonally changing environment, from the well- the stratification, deeper wind mixing, and the restora- mixed, nutrient-replete starting condition, through the tion of the depleted nutrients: by the late autumn, dia- slow resource depletion of the spring period, and the toms, including Aulacoseira and Asterionella, are gener- rapid depletion after the onset of stratification. Finally, ally the most abundant algae, dominating the shrinking the effect of enhanced mixing weakens the light income residual biomass. but gradually restores the resource base. The partial independence of the two axes is conveniently empha- sized by the inclusion of the winter ‘‘loop’’ when the light income falls below a level that will support new growth, while the system may be accumulating new external resources, only after I** has increased to the point where net growth can be supported at the cost of net resource reduction. The development continues by the imposition of the trajectory on the plot showing the distribution of the morphological traits of the algae (Fig. 3B); as these prove such useful predictions of physiological perfor- mance, which, in turn, anticipate their ecologies, the fit should not be surprising. Nevertheless, the correla- tion of function and the dynamic response to environ- mental change is an extremely satisfying one. It will

FIGURE 3 (A) How growth conditions in a monomictic deep lake (mixed in winter) track through a calendar year, selecting sequentially for a low-light tolerant spring bloom (of R species), then opportunist C species after the onset of stratification, leading to the biologically enhanced segregation of nutrient resources tolerated by S species, before autumnal downmixing again forces conditions back toward the top right: nutrients may be further increased (by inflow) in winter, when primary production is still increasingly light limited. (B) Some of the algal species that might be selected are shown in an analogous matrix that is based purely on shape- and size- characters of the algae concerned (svϪ1 versus msvϪ1, where s is the surface area of the alga in Ȑm2, v is its volume in Ȑm3, and m is the maximum length dimension, in Ȑm). A strong correlation exists between the morpholo- gies of these algae and their functional ecologies. The algae shown are represented as follows: Ana ϭ Anabaena flos-aquae, Ank ϭ Ankis- trodesmus falcatus, Aph ϭ Aphanizomenon flos-aquae, Ast ϭ Asterio- nella formosa, Cer ϭ Ceratium hirundinella, Chla ϭ Chlamdomonas, Chlo ϭ Chlorella, Cry ϭ Cryptomonas ovata, Din ϭ Dinobryon di- vergens, Eud ϭ Eudorina unicocca, Fra ϭ Fragilaria crotonensis, Lim r ϭ Limnothrix redekei, Mel ϭ Aulacoeira subarctica, Mic ϭ Microcystis aeruginosa, Mon ϭ Monodus, Pla ag ϭ Planktothrix agardhii, Per ϭ Peridinium cinctum, Rho ϭ Rhodomonas pusilla, Scq ϭ Scenedesmus quadricauda, Sth ϭ Stephanodiscus hantzschii, Syn ϭ Synecococcus, Tab ϭ Tabellaria flocculosa, Vol ϭ Volvox aureus. 584 PLANKTON, STATUS AND ROLE OF provide us with one of the most important clues to tend to combine intensive mixing with renewed re- understanding how local diversity is maintained in sources and to select species in the C-R intermedium nature. through much of the year: Gyrodinium spp., Alexan- drium tamarense, Thalassiosira leptoporous can be typi- cal assemblage members. Away from the epicenters of D. Traits in the Marine Phytoplankton the upwelling areas and where, indeed, the water is less Before that, however, it is necessary to establish that mixed but still charged with nutrients, such dinoflagel- the rest of the planktonic biota respond to environmen- late taxa as Dinophysis, Gonyaulax and Gymnodinium tal cues in broadly analogous ways. Marine phytoplank- catenatum provide prominent markers of the (R-S) tran- ton would seem appropriate for first consideration. Evi- sition between stressed and disturbed conditions. dence of a similar coherence among morphological form, physiological performance, and population re- sponses to environmental forcing was presented in Mar- IV. FORM, FUNCTION, AND galef’s (1978) seminal discussion of plankton life- SELECTION IN THE ZOOPLANKTON forms, while the insights underpinning the ‘‘mandala’’ model (Margalef et al., 1979) continue to intrigue A. The Basic Adaptations of plankton ecologists. Nevertheless, the apparent func- tional and morphological correlations have scarcely Planktonic Animals been quantified. Preliminary considerations of the types In the terms of species success, the survival strategies, of phytoplankton characterizing the various subdivi- and selective biases, the ecological constraints govern- sions of the sea (Fig. 2), however, do reveal entirely ing the lives of phagotrophic zooplankton are wholly parallel trends between morphology and performance. analogous to those acting on the phytoplankton. Spe- For instance, as days lengthen over the open seas of cific requirements differ substantially, as do the time- the temperate latitudes, an initial typical spring bloom scales over which the organisms respond to environ- of such chain-forming diatoms as Thalassiosira norden- mental fluctuations. The essential requirements of the skioldi, Skeletonema costatum, and Chaetoceros (all man- phagotroph are to be able to encounter and capture ifestly having R-type, attuning characters) gives place sufficient appropriate food to supply the elemental as- in summer to relatively large, motile, S-like peridinians sembly of its biomass, to maintain and defend that (e.g., Scrippsiella trochoidea) and ceratians (e.g., biomass and perpetuate its genetic instructions, and to Ceratium tripos), which are often followed, in autumn, secure the energetic demands of the relevant processes. by chain-forming (Chaetoceros spp.) or needle-like (Rhi- Resource adequacy for nonphototrophs may be judged zosolenia) diatoms with high surface-area-to-volume ra- principally in terms of the availability of ingestible par- tios and antennal enhancement. In the high-nutrient, ticulate biomass (living or detrital), being the only prac- high-energy waters of coastal margins, potential domi- tical source of reduced carbon, although the judgment nants are generally small, usually unicellular, centric of organic-resource quality must acknowledge the ca- diatoms (e.g., Cyclotella caspia, Thalassiosira weiss- pacity of its blend of proteins to fulfill the biochemical flogii), green flagellates (e.g., Dunaliella, Nannochloris), requirements for nitrogen, phosphorus, sulphur, iron, euglenoids (Eutreptia), and gymnodinioids (Gymnodi- and so on. Resource gathering, whether essentially her- nium); all qualify as fast-growing opportunist (C-) spe- bivorous, carnivorous or detritivorous, or whether ac- cies. The estuarine prorocentroids are also conspicuous. tively hunted or sedentarily filtered, carries a high en- Blooms of Phaeocystis may follow, before giving place ergy demand: ‘‘maintenance costs’’ of phagotrophs are to ceratians. In the highly stratified, tropical oceans, proportionately high, not untypically accounting for dominance passes quickly from diatoms to Emiliana some 90% of the resources consumed. The energy and to the large Ceratium spp. and Ornithocercus. The comes from the original photosynthetic investment in big, buoyancy-regulating, stress-tolerant, S-species of carbon bonds, whose controlled oxidation sets the prin- diatom (Ethmodiscus) and dinoflagellate (Pyrocystis) are cipal processing constraint in animals, which is to sup- at the culmination of this sequence. ply the tissues with sufficient oxidant. Spatial differences—among latitudes or between ne- In terms of the lives of planktonic animals, already ritic shelf waters and the open oceanic systems— contending with the problems of operating in a fluid, probably also attest to the functional differentiation of viscous medium, the key issues are still about staying the phytoplankton. Areas of frontal activity and of sur- alive, about finding adequate amounts of suitable foods, face upwellings of the deep oceanic circulation currents with a sufficiency of individuals reaching reproductive PLANKTON, STATUS AND ROLE OF 585 age, and about having the collective residual fecundity dent assessment of the expression of ‘‘resource-stress to be able to recruit the next generation. The size range tolerance,’’ ‘‘exploitative invasiveness,’’ and ‘‘distur- of planktonic animals embraces the flagellated protis- bance tolerance’’ among animals. In this way, it is possi- tans (whose phylogeny merges with the dinophycean, ble to fit planktonic animals to a habitat template, analo- synurophycean and euglenophycean mixotrophs, and gous to that for the phytoplankton, on the basis of a photoautotrophs), whose dimensions leave them sub- wholly functional classification. stantially embedded within the viscous range of aquatic environments, through to crustaceans and young fish whose lives reach well into the turbulent range. B. Life-History Strategies Whereas the former rely on encounters of suitable food The resident zooplankton of the open seas and of larger particles (organic detritus, not necessarily autochtho- oligotrophic lakes live in environments where the pro- nous, bacteria, small algae) within the same viscous ducer biomass is chronically resource limited: the po- neighborhood, animals living mainly within the bound- tential food resources for zooplankton (planktonic al- aries of the turbulent world have a modicum of control gae, bacteria, and particulate organic detritus) are over their own movements. They also exploit turbu- generally Ͻ 0.1 g C mϪ3. To be successful under persis- lence in their foraging by generating local circulations tent conditions of dilute resource, animals must blend entraining small food particles (Margalef, 1997; Roth- energy-efficient foraging with controlled resource ex- schild and Osborn, 1988). ploitation—they must adopt the ‘‘patient’’ strategy of Within this general scheme of classification, there resource-stress tolerance, especially with respect to the remain numerous opportunities for differentiation of recruitment of juveniles. Investment in a small number foods and foraging mechanisms, as well as substantial of relatively large eggs with a relatively long develop- feeding specialism, especially among the rhizopods and ment time is typical. Physical and behavioral defenses the rotifers. There is also considerable differentiation reduce the vulnerability to predation. Such traits distin- among the strategies for survival and resource exploita- guish the life histories not only of Diaphanosoma but tion. In addition, predation by planktivorous fish and of many of the calanoid copeods also. The sophisticated invertebrates has a central role in structuring zooplank- browsing mode of feeding they adopt has been shown to ton assemblages: whereas larger animals ostensibly have be sufficient to sustain natural populations and support more foraging opportunities for a wider choice of poten- their reproduction at food concentrations in a range tial foods, they are also more vulnerable to visual preda- equivalent to 0.01 to 0.08 g C mϪ3 in both the sea tors (Brooks and Dodson, 1965; Hall et al., 1976). The (Huntley and Lopez, 1992) and lakes (Hart et al., 1996). latter is readily demonstrable in experiments, but the For reference, a producer biomass of 0.08gCmϪ3 may part played by food preferences and availabilities has be supported by photosynthesis in a mixed layer of proved less tractable. However, Romanovsky’s (1985) Յ60 m (i.e., Յ5gCmϪ2), so long as the microbial analysis of life-history strategies of the planktonic Cla- loop is able to maintain a bioavailable nutrient base docera distinguished among those species that invest in exceeding 0.1 g P and1gNmϪ2). Arguably, the ciliates high survivorship rather than in rapid juvenile growth (e.g., Halteria, Strombidium), which constitute a sig- (exemplified by Diaphanosoma brachyurum), those ulti- nificant part of the diet of calanoids in oligotrophic mately large-bodied species that sustain rapid rates of lakes, must be, similarly, stress-tolerant patient strate- juvenile recruitment and development (typified by gists. Daphnia hyalina), and those smaller-bodied, fast-repro- In the more productive waters of fertile lakes and ducing inhabitants exploiting the fluctuating opportu- rivers, estuaries, nutrient-enriched coastal-shelf waters, nities of temporary ponds and water bodies (including and oceanic upwellings, the capacity to support autotro- species of Moina). Taking particular account of the in- phic biomass may, for some of the time at least, signifi- terspecific trait variability in adult cladoceran size and cantly exceed 0.1 C g mϪ3. This is an approximate the negative correlations (‘‘consistent tradeoffs’’) be- threshold, above which the energetic return from filter- tween egg number and yolk investment and between feeding becomes steadily more favorable. Among lakes, larval development time and resistance to starvation, for example, Daphniids tend to become much more Romanovsky recognized three basic life-history strate- abundant, absolutely, and relative to calanoids. Most gies. Following terminology attributed to L. G. Rame- species of Daphnia, when adequately nourished, are able sky, he referred to these as being ‘‘patient,’’ ‘‘violent,’’ or to grow and mature rapidly, to increase egg production ‘‘explerent.’’ It needs little insight, however, to recognize and to recruit the next filter-feeding generation over a that this imaginative perception is but a quite indepen- few days (George and Reynolds, 1997). The 12-fold 586 PLANKTON, STATUS AND ROLE OF increase in the Daphnia-dominated community-filtra- Modern molecular approaches are slowly sorting out tion rate in 13 days, measured by Reynolds et al. (1982; ‘‘who does what’’ but, for the present, the diversity of note, aggregate filtration capacity doubles every 3 to 4 the bacterioplankton is anticipated to be high. days), conforms to the understanding of an exploitative, Among oxic freshwaters, the free-living bacteria are or ‘‘violent,’’ life-history strategy. Among the noncrusta- known to include members of the coccoid and rodlike ceans, the ciliates of microaerophilous environments Bacilli, the Flavobacteria, Pseudomonads, and Vibrios (e.g., Metopus, Caenomorpha) react in an analogous way (Atlas and Bartha, 1993). All are heterotrophs, which to a food abundance in media from which other sorts exploit sources of biogenic organic carbon. These of consumer are mainly excluded. sources were always recognized to constitute the waste Many noncrustacean members of the zooplankton products and cadavers of the biotic components of the take advantage of short generation times to track bursts aquatic system generally. As understanding of pelagic of algal or bacterial abundance. Protists including Dif- carbon metabolism has developed, it has become possi- flugia, Coleps, Tintinnidium, and Nassula and rotifers ble to separate the active role of microbial heterotrophs such as Keratella, Kellicottia, and Brachionus will often in transferring dissolved organic compounds derived respond to an expansion in suitable algal foods, but this from low-molecular weight, mainly algal photosyn- occurs before the Daphniids can ascend to dominance. thetic intermediates (especially dissolved glycollate), Their disturbance-accommodating lifestyles are well as the food supply to the flagellate—ciliate—copepod suited to the direct exploitation of small phytoplankton trophic links, from that of degradation of biogenic par- and organic detritus in the middle reaches of large riv- ticulates (organic detritus, fecal pellets, etc.), usually ers, provided travel times permit (Viroux, 1997). by sessile or stalked bacteria, such as Caulobacter, acti- nomycetes, and fungi, that attach to the particles and whose activities liberate carbon dioxide and mineral nutrients into the water. Both contribute substantially V. FUNCTION IN THE to the cycling of carbon and nutrients, but in contrasting BACTERIOPLANKTON ways. Oxic breakdown of abundant biogenic material releases resources to the autogenic synthesis of new Microbial populations constitute the third integral com- mass. The phagotrophs of the microbial loop depend ponent of the planktonic communities of lakes and seas, on the close coupling that the viscous scale facilitates, where they are often numerous (typically within the but most of the energy is consumed internally and the range 105 to 107 cells mlϪ1). Microbial diversity, how- material transferred to higher trophic levels is abso- ever, is not yet well understood, principally because lutely small. the bacterial taxa are still insufficiently distinguishable In smaller lakes and ponds, the nature and diversity to be separated routinely to species level. For many of organic carbon sources are enriched by direct trans- years, bacteria have been identified as much by what port of biogenic materials from the catchment area. they do as by their morphological affinities. Given that, However, current understanding is also having to ac- for most of them, the utilization of dissolved reduced- commodate the recognition that often the largest frac- carbon substrates provides the main source of energy, tion of organic carbon present in stream and lake waters even the functional approach appears to have its limita- comprises plant-derived humic and fulvic acids washed tions for bacterioplankton. ‘‘Organic carbon com- in from catchment soils (Wetzel, 1995). They are partic- pounds’’ are derived from a very wide range of the ularly abundant, of course, in brown and ‘‘black’’ waters breakdown products of biogenic materials, many origi- draining forests and peatlands The relative size of this nating from the land, as well as a host of very unnatural fraction indicates its high resistance to microbial break- anthropogenic organic substances. The ability to break down; it persists in measurable amounts in the largest down particular classes of compounds or kinds of bonds oligotrophic lakes and even in the open oceans. Refrac- is unlikely to be shared by all bacteria. Every such tory dissolved organic carbon from terrestrial sources process presumably requires the action of one or more does break down slowly; some is rendered labile by discrete enzymes, and the ability to produce each en- exposure to ultraviolet radiation. zyme requires one or more genes dedicated to its pro- Away from aerobic mixed layers, freshwaters furnish duction. As the genetic complement of microbes is rela- other microhabitats exploitable by bacteria. In the mi- tively modest, it follows that the number of separate, croaerophilous environments of the bottom sediments substrate-specific bacterial strains is likely to be high. and in the deep water of stratified, productive lakes, PLANKTON, STATUS AND ROLE OF 587 anaerobic microbes are common and typically numer- the metabolic constraints set by the redox en- ous; they include Clostridium, the sulphate-reducing vironment, are presumed to be decisive in species distri- Desulfovibrio, and the Archaean Methanogens. Inter- butions. acting gradients of light and of redox superimposed on relatively stable density gradients may also provide vertical sequences of microhabitats, each niche poten- tially differentiated according to the microorganisms it VI. TEMPORAL PATTERNS IN THE supports and whose physiological adaptations it most ORGANIZATION AND DIVERSITY OF suits. To be able to carry out photosynthesis in a reduc- PLANKTONIC COMMUNITIES ing environment favors Rhodospirillum; but to be able to use sulfide or sulfur, as photosynthetic electron do- A. Quantifying Structure in nor, can bias the selection in favor of Chromatiaceae and Chlorobiaceae). The involvement of specialist Planktonic Communities chemolithotrophs in nitrification (Nitrosomonas, Ni- This survey of the wealth of species to be found in the trobacter) and in the oxidation of sulfur (e.g., Thiobacil- plankton serves to emphasize the collective breadth of lus, Beggiatoa) and iron compounds (Ochrobium) fur- the adaptive specialisms themselves but which, individ- ther adds to the microbial diversity of freshwaters. ually, provide advantage only to the certain species that In the open waters of the sea, most bacteria are possess them and only at the certain times when the aerobic—relatively few anaerobes are ever found in the specialism affords some operational benefit over others surface waters. Many of the same genera represented that do not have them. A reasonable deduction that in freshwaters include marine species: Pseudomonas and may be made is that the collective diversity of plank- Vibrio are often found to dominate and species of Flavo- tonic species reflects the number of distinctive habitats, bacterium, Alcaligenes, and Cytophaga are found in high or niches, that it is possible to define. This is, roughly, numbers (Atlas and Bartha, 1993). Sediments receiving the niche differentiation theory of biodiversity: every organic inputs are bacteria-rich; moreover, where these species has an optimum performance, which is facili- fall anaerobic, marine sulfate-reducers and methano- tated when each of the component processes is at the gens are present in substantial numbers. species-specific optimum. When the conditions simul- In both marine and freshwaters, the vital contribu- taneously satisfy all the species-specific optima of a tion of the bacterioplankton to ecosystem function given species, then that species is uniquely favored to arises not only from the mineralization of organic car- outperform all the others for which the niche conditions bon products but from the potential remobilization and are suboptimal. There can then be as many successful renewed bioavailability of nitrogen, phosphorus, and species as there are tangible niches, for each stands to the metals required in the assembly of new biomass. be the fittest competitor under its favored blend of Most bacteria are supposed to be capable of rapid environmental conditions. This means that in any given self-replication, with the potential to undergo several niche location, the local diversity is likely to be actually doublings per day. The relative ease of dispersal contrib- quite low. utes to their apparent ubiquity and to their fidelity to An alternative view might be moved to accommodate appropriate habitat opportunities. Microbial biomass is, the observation that local diversity is sometimes actu- nevertheless, clearly subject to environmentally im- ally quite high, even when the available niches seem posed rate and capacity limitations. In many instances, to be few in number (this, it will be recalled, was Hutch- their requirements are not dissimilar from those govern- inson’s paradox). It should also accommodate another ing the growth of photoautotrophs. However, small cell of the observations emphasized in the foregoing sec- size and superior uptake kinetics favor the perfor- tions—that is, there is a great deal of temporal environ- mances of bacteria. A greater collective versatility in mental variability, sufficient, indeed, to move the selec- the energetics and potential sources of reductant and tive advantage from one species to another, often before oxidant opens up more of the aquatic environment to any has been able to assert its competitive dominance. chemotrophs than to phototrophs. The distinguishing Sometimes, moreover, the variability is plainly driven dependence is the one for appropriate organic carbon externally, beyond organisms’ power to regulate—the skeletons. Their availability remains the regulation changes are brought about by physical forcing with on the numbers and dynamics of planktonic bacteria. sufficient magnitude to ‘‘disturb’’ the existing internal The nature of the carbon compounds, together with organization. At the appropriate intensity and fre- 588 PLANKTON, STATUS AND ROLE OF

ϭ Љ Љ quency, such disturbances might provide a mechanism interspecific distribution, E H /H max, is itself a use- for rotating the competitive advantage among species ful measure. and for maintaining local diversity. This, indeed, is Local species richness (the sample, the pond, the the essential basis to the main counterview to niche- lake) may run to a few tens of phytoplankton and, if differentiation theory. the phagotrophic protists are included, perhaps 100 or Two further features of the present appreciation of so species of zooplankton. Regular sampling may raise planktonic communities that are attractive to the stu- this total considerably, as seasonal changes are encoun- dent of biodiversity have also been noted in the survey. tered and the probability of encountering rare species One is the planktonic timescale: the frequency of gener- is increased (Padisa´k, 1992); ‘‘rare’’ in this context may ations allows the rates of internal compositional mean one individual per liter, but there could still be changes (competition, succession, predation) to be a billion such individuals in a small, 10-ha lake. As measured and the resistance to external forcing, as well observed earlier, most (Ն95%) of the total biomass of as the resilience to recover from forcing, to be quantified phytoplankton and that of zooplankton will each be (Reynolds, 1997a). The other is the quantitative infor- invested in eight or fewer species. Most of the consider- mation that is now available on the performance capaci- ation of evenness concerns how the total biomass is ties of representative planktonic organisms—from their shared among those eight. Thus, whether local species resource thresholds to their resource-regulated re- composition is species rich or otherwise, the perception sponses and the onset of their resource-saturation. of its diversity is greatly affected by the relative evenness These help us to distinguish internal structural changes of the most common species. from externally forced restructuring and to express Often without clear confirmation, the issue of ‘‘pro- them in energetic terms. In this section, we may deduce tecting biodiversity’’ generally extends to the totality of why the two main theories of biodiversity are not at all species, or the totality of species that could live in mutually exclusive and when we may presume either a particular habitat (Wilson and Peter, 1986). Unlike is valid. To do this, however, it is necessary formally diversity, it has no formal mathematical expression. to distinguish between the diversity of community However, we may quickly recognize that if a single structure at a given location and the richness of species patch of the aquatic environment—say, the open water present among a series of such locations at the regional of a 10-ha lake—can furnish habitat sustaining viable or even global level. populations of a few tens of species of planktonic spe- cies, then a great many such ponds must exist if all the species are to be supported, many of which will be B. Quantifying Diversity in common to a wide selection of the water bodies. Planktonic Communities In this way, two questions need to be answered. The first is about the mechanisms by which within-patch Diversity is a concept drawn from communication the- diversity is upheld, against the tendency for the opti- ory (Shannon, 1948), referring to the amount of discrete mally adapted functional specialists to exclude its com- information in a particular location. In communities, petitors. The second questions the mechanisms by it could refer to the different fragments of genetic infor- which between-patch diversity is maintained, so that mation. A diverse community is one with many different individual species have more opportunities to maintain kinds of genes (species) present simultaneously. This stocks at viable and sustainable levels. biotic diversity (HЉ) can be quantified with great preci- sion, using the specialized Shannon-Weaver function: C. Assembly and Autopoiesis of Communities The essential step in logic that separates the niche- Diversity increases with the number of species (s) diversification and the persistent-disturbance theories each contributing biomass (bi) to the total, B, in the of species richness rests on an acceptance that the sup- sample of lake or seawater. The more species present, portive capacity is not always filled; conversely, al- Љ ϭ the greater is the diversity, until H max log2 s.In though the capacity of the resources is always finite, practice, it is necessary to set a bar on the efficiency of the underexploited resource base is, by definition, not search for the rarer species (more diligent searchers and ‘‘limiting.’’ Many students of the phytoplankton persist more expert taxonomist-hunters would always score in comparing the quantities of nutrients in the water higher diversities). Nevertheless, the evenness of the relative to the ideal composition of algal biomass, then PLANKTON, STATUS AND ROLE OF 589 judging that the nutrient in least supply is ‘‘the limiting petitor in Aesop’s fable, the tortoise or the hare? When factor.’’ That phytoplankton concentration is ever able a lake, just like Crose Mere (discussed earlier), stratifies to increase at all is because, in reality, there are times in April or May, it opens the stage to many more players. when nutrient resources are available to support the Is it not those species, such as Chlorella, Rhodomonas, additional biomass and unharvested light energy to fuel and Cryptomonas that can grow relatively rapidly, by its assembly. Moreover, these opportunities are attribut- virtue of their C-type morphological and functional able to natural fluctuations in the resource base: the biases, which actually do so (perhaps doubling mass spring increase in temperate waters, the most conspicu- every 24 hr) to become initially prominent? Many field ous feature of lakes and seas at higher latitudes (Fogg, data (considered by Reynolds, 1984a; Sommer, 1981) 1965; Sverdrup et al., 1942) is the consequence of point to the simultaneous growth of other species, of lengthening days and strengthening insolation of wa- Ceratium, Peridinium, and Microcystis, for example, but ters, which have themselves demonstrably been re- at maximal rates that are far slower than those which charged with nutrients during the winter months of Chlorella can attain. The tradeoff for invasiveness is hydraulic circulation and augmentation from inflow, at acquisitiveness—though the relatively large, motile the same time as meeting low biological demands. The life-forms of acquisitive, stress-tolerant algae stifle rapid spring bloom, at least initially, is the response of the conversion, such that some four to five days may be producer community to an expanding capacity of the needed to achieve each biomass doubling, yet they do resource and energy bases. Later in the year, the re- not sink out and they are too big for most planktonic source supply may well fail to meet the biological de- phagotrophs to ingest. The slowly assembled biomass mand and severe constraints are them imposed on its is carefully conserved and, in some cases, protected by further growth and maintenance. Alternatively, it is left elaborate chemical defenses. By exploiting the structure to shortening days and convective mixing in the autumn of the water column to the capacity of its resources and months to erode the supportive capacity of the insol- by continuing to grow for longer, often in the face ation flux. We will return later to the subject of these of intensifying resource shortage, the S-type adaptive constraints but, for the moment, it is important to con- strategy allows the organisms to achieve a larger, cli- sider in more detail how the phytoplankton behaves mactic biomass than that achieved by any of the earlier when its production is not limited by nutrients and invasive species. The fact that the dominance can be- when the production of zooplankton leaves large come total, other species are effectively excluded by amounts of phytoplankton relatively still unharvested. the ultimately superior competitor and the Shannon The organismic responses to the opportunities provided diversity falls to a minimum, is fully in keeping with the by a luxury of supply in all resources are instrumental anticipated outcome of events within the pelagic niche. in molding the structure of ascendent communities. Another relevant observation, that relatively few spe- The key feature of an expanding (or merely replete) cies ever attain such outright dominance of the phyto- resource base is that its exploitation is relatively plankton, leads to the deduction that there are many straightforward. Species do not compete for the re- routes of internal change but few ultimate outcomes. sources in the sense that their garnering by the individu- This last point is taken to be a powerful indicator of als of one species denies an adequacy of the nutrients the system’s ability to self-organize, a measure of its simultaneously supplied to the individuals of a second autopoiesis. This is a property of all ecosystems or an ith species. The only question of ecological impor- (Jørgensen, 1992) but its mechanical basis is not well tance is ‘‘Can it obtain enough?’’ This is not to say understood. However, the further examination of the that opportunistic ‘‘luxury uptake’’ and resource storage processes of capacity-filling behavior of the phytoplank- might not become important at some later juncture, ton yields a conceptual and preliminarily empirical view only that species 2 to i can also perform to their capabil- of internal organization. If the developmental progress ity at the same as species 1 is also performing. Neverthe- of a producer-dominated pelagic system is considered less, rapidity of growth and reproductive efficiency are against axes representing the standing crop (in units crucial to the exploitative outcome: having a large start- of organic carbon) and the harvest of photosynthetically ing inoculum and, especially, a high yield/resource con- active radiative flux (in W mϪ2 or J mϪ2 dϪ1), then the version potential is vital to the fitness of colonist and coordinates corresponding to the ‘‘open stage’’ at the invasive species. If we judge it to be ‘‘outcompeting’’ the start of the summer stratification may be set close to slow-growing species present, we are giving a second the origin (Fig. 4A). The standing crop is far below nuance to the word ‘‘competition.’’ Really, we need an- the potential of the resource-limited carrying capacity other word, perhaps ‘‘fitness’’: who was the better com- (horizontal axis) and thus is collectively capable of 590 PLANKTON, STATUS AND ROLE OF

FIGURE 4 (A) A simple plot to show the maximum light that can be harvested by a given biomass of planktonic algae relative to the energetic costs of its maintenance and loss rates; the difference is the exergy of the system. For a time, developing systems increase biomass and exergy, until the reduction in the exergy cushion leaves them increasingly sensitive (B) to fluctuations in the harvest-determined carrying capacity; (C) resource limitation truncates the cushion but the ‘‘sail shape’’ (D) can be used to subsume the triangle from Figure 3. intercepting very few of the photons that penetrate the munity with the physiological performance of a Chlo- water surface before their energy is absorbed by the rella culture, the unimpeded biomass-specific light water. The notion of capacity filling is that the structure harvesting and carbon fixation rates are able to accumu- will move away from the origin and toward the upper late new cell carbon sufficient to double or possibly right corner, whose coordinates are determined either quadruple the plant biomass within 24 hr. It is possible where all of the least available of the resources has to suppose, in these early developmental stages, that been incorporated into biological standing crops (the the doubling of the biomass will roughly double the resource capacity) or where every available photon is area of light harvesting surface, so the coordinates rep- intercepted by planktonic light-harvesting centers and resenting the supportable biomass move upward and is driving photosynthetic carbon reduction (the pro- rightward. The new biomass incurs an increment in cessing capacity). If we now imbue our producer com- respiratory losses, so the coordinates representing the PLANKTON, STATUS AND ROLE OF 591 maintenance costs—assumed, for simplicity, to be di- income without resorting to a restructuring of the rectly proportional to the biomass—diverge from the biomass. slope of the harvesting capacity. Given strong light and Because we have defined this cushion in terms of a steady water temperature, producer biomass begins energy exchanges, it is appropriate to refer to it in to increase exponentially. It is predictable that, as accu- thermodynamic terms—it is the exergy of the system mulation proceeds, the light- harvesting centers are in- (Jørgensen, 1992). We may see at once a presumption creasingly probable to be shaded (meaning that even that a high income flux relative to biomass maintenance with no diminution in the surface flux, individual light- favors exploitation by species that can build the highest harvesting centers are activated less frequently). The levels of harvesting capacity for the biomass—that is, provision of additional biomass is no longer rewarded those which contribute most to a high level of exergy. with proportionate energy harvest. However, high net fluxes are not reliable and energy The limiting condition is approached when the main- harvesting is ultimately sensitive to changing day length tenance of the expanded biomass consumes all the en- and solar elevation and to the variability of cloud cover ergy it is able to capture. This biomass, shown by the and atmospheric absorption and scatter, all of which broken line in Fig. 4A, is the maximum that can be affect the daily flux of harvestable energy penetrating supported. The coordinates are proposed on the basis the water. Moreover, atmospheric variability also in- of photosynthetic and respirational properties solved cludes the work of wind and the impacts of varying for Chlorella and the highest daily aggregates of light dissipation rates on the mixed-layer depth and, hence, income daily income of photosynthetically active radia- the mean exposure of entrained plant biomass to har- tion that can be realistically proposed (12.6 MJ mϪ2 dϪ1; vestable energy. 10.5 mol C mϪ2) through relationships developed in The reality of biomass assembly and its additional Reynolds (1997a). energy-harvesting capacity is that they have to be con- ducted against a background of a stochastically chang- ing energy income. Intriguingly, the components of the D. System Exergy and Disturbance relationship are provisionally quantifiable in energetic The precise quantification of Fig. 4A may be misleading terms, at least probabilistically, if the energy harvest is and not universally applicable. This is less important, solved as the mean biomass-specific photon capture by however, than the form of the traces of the maximum plants entrained in the mixed-layer circulation (Reyn- light-harvesting curve and the maintenance diagonal olds, 1997a). In this way, the temporal fluctuations and of the geometrical shape that they bound. It repre- in the harvestable income can be represented as an sents the only part of the plot in which population irregularly oscillating time track (the broken line in growth can be sustained. Above it is a void of underpop- Fig. 4B). High values correspond to intense photon ulated opportunity (exploitation of which requires the fluxes into clear or shallow mixed layers, low points to expansion in the light-harvesting capacity by increasing overcast skies or strong wind-forcing and mixed-layer producer biomass in the rightward direction); below is deepening. We may also recognize that the externally an area representing unsustainable biomass in excess forced depression of the harvestable energy flux may of the current energy income (far from being able to still be sufficient to meet the biomass maintenance cost, increase its total biomass, the system here must shed with a little in hand to maintain positive increase—that biomass, so that the maintenance of what remains is is, the fall in income is absorbed by the exergy cushion: brought back within means of the current energy flux the structure survives and has the resilience to recover to sustain). In this way, the spring increase of phyto- promptly to its maximum capacity when the harvestable plankton is represented by a rightward response of bio- energy flux is restored to an optimum and the capacity mass to an upward income in harvestable energy, with to expand the biomass is fully restored. On other occa- the increase in light harvesting capacity moving diago- sions, however, especially once a substantial standing nally upward and rightward in consequence. By anal- biomass has been put in place, the flux of harvestable ogy, the autumnal decline in biomass is a leftward energy falls below the minimum maintenance require- response to regain balance between now-high ment. The cushion of exergy is exceeded; the energy maintenance costs against a diminishing energy in- needs of the system are now out of balance with its come. The excess of energy-harvesting capacity over supplies and are fundamentally unsustainable. This sit- the costs of its maintenance provides the existing crop uation cannot persist for long before there has to be a with a second asset—a cushion of capacity that can reduction in the standing biomass, back to a level that absorb the impact of short-term variability in the energy is energetically sustainable. There is abundant resort 592 PLANKTON, STATUS AND ROLE OF to minimal metabolism, including the production of tonic succession. Plainly, the curved upper surface cor- resting spores and propagules, through to mass mortali- responds to the C-S axis of increasing structural devel- ties of vegetative cells. The biomass response is sharp opment, increasingly subject to resource competition and severe, conforming to all conventional apprecia- and powerful selection. In contrast, the maintenance tions of an externally forced disturbance reaction. axis is the lower boundary of the adequacy of the exergy Following the course of irregular forcing episodes, flux to drive the assembly of the community. Thus, the represented in Fig. 4(B), it is easy to appreciate that lower boundary of the ‘‘sail’’ represents the extremes planktonic systems are far more liable to restructuring of disturbance tolerance permitted by the attuning R- disturbances than they are to achieve their autopoetic strategy. The two straight boundaries could equally be potential of a low-diversity, competitively excluded cli- scaled in terms of K** and I**, the rightward trend max to the succession. This maturation process is sim- representing increasing resource limitation, the down- ply overridden by the frequency of externally forced ward trend corresponding to carbon-processing limita- disturbances that it rarely, if ever, proceeds to its logical tions. The axes serve just as well in separating the outcome. It may also be seen that the intervention of animal analogues of food supply and resource stress weather fluctuations and events, superimposed on pre- and ‘‘explerent’’ opportunism provided by externally dictable climatic cycles, is a, if not the, principal agent imposed disturbance. Subject to current methodologi- resisting exclusion and local extinction of planktonic cal uncertainties, there seems to be every probability species and contributing to Hutchinson’s paradox of that analogous axes describe the availability of organic local species richness. Steady states are just so rarely carbon sources and processing opportunities for micro- achieved that species are retained, at least at the scale of bial plankton too. Note also that the fluctuating coordi- plankton generations, in a nonequilibrium coexistence. nates of stochastically variable environments continue Here, at least, is a candidate mechanism contributing to fall both within and beyond the sail area defining to the maintenance of a high biodiversity in the plank- positive growth responses; only when the track is kept ton. We should pursue its workings a little further. firmly and persistently in the S or R areas of the plot is there likely to be fierce and ongoing competition leading to the progressive installation of a single species, E. Resource Limitation and Diversity dominating a low-diversity, low-equitability commu- Long before most pelagic systems can approach the nity. On the other hand, for as long as externally driven attainment of a producer base at the capacity of the variability keeps resetting the coordinates of the envi- harvestable energy flux, biomass assembly will have ronmental conditions, at least with respect to the chosen been constrained by the capacity of the bioavailable axes, the time track keeps moving freely and extensively nutrient resources. We can represent this constraint across and beyond the body of the shape, signifying very simply by superimposing the vertical axis across that conditions rarely exist for sustained competition the exergy cushion (Fig. 4C). Between the origin and to last either for long enough or in one direction for the resource limit there remains an opportunity for any of the species present to have sufficient chance biomass fluctuation but, against the vertical axis, the to deploy its superior adaptations to the competitive assembly opportunity remains strictly within the defi- exclusion of others. nition of exergy. Thus, the area of the plot correspond- ing to sustainability of growth (Fig. 4A) is finally shaped as in Figure 4D. VII. MECHANISMS PROMOTING The new geometric figure is without a name—the AND MAINTAINING DIVERSITY best likeness I can think of is the sail of a windsurfer. Its periphery, however, readily corresponds to quantities IN THE PLANKTON established in sections III–V: the abundance of re- sources, relative to the consumptive demand, favors A. Diversity within Habitats the advance of the most exploitative species, whose The geometric representation of environmental vari- geometric range spreads from the origin along the line ability and of its impact on species selection may prop- of the maximum biotic exergy flux. The closer this erly be pursued in relation to the exergy model, but it approaches the capacity of the resources, the greater is is actually easier to bring the concept of fluctuation the stress of resource deficiency and the greater is the tracking back to the habitat template (of Fig. 3A), be- adaptation required to exploit it. Maintaining a high cause it is easier to relate to the environments it seeks exergy flux remains the strongest driver of the plank- to represent (Figs. 1 and 2) and because sufficient pre- PLANKTON, STATUS AND ROLE OF 593 liminary knowledge exists about how the tracking thus substantial within-season variability will lead to almost represented actually selects for the preferred traits of chaotic short-term time tracks, such as the fragment species, at least of the freshwater phytoplankton (Fig. included in Figure 5C. 3B). To be clear, the resource- and energy-replete condi- Our deduction is again that the effect of environmen- tions, wherein resources fully meet present organismic tal variability is to move any selective advantage among demands, are represented in the upper right-hand cor- species at a faster rate than autopoesis narrows the ner of the template. Of those present, the species most opportunities or that competition can forge a low-diver- advantaged are the opportunistic, invasive C-type spe- sity monoculture dominated by a single well-adapted cies (like Chlorella; see section III.B and Fig. 3B). Bio- species. We know that this theoretical outcome, cor- mass growth creates a strain on the readily available rectly anticipated by Hutchinson (1961), certainly is resources, more elaborate resource gathering is re- achievable and good descriptions of local, competitively quired, and autopoesis favors a succession to more con- excluded community structures are described in the servative, accumulative S-type dominants (like Micro- literature. These cover the sort of arrested ‘‘plagiocli- cystis) with a high tolerance of resource-supply stress maces’’ of overwhelming Microcystis dominance of trop- and a resistance to disturbance. Large size becomes ical eutrophic Lake George (Ganf and Viner, 1973) and selectively valued but at the tradeoff in terms of surface- imitated in several field-scale enclosure experiments to-volume ratio (Fig. 3B) and at the price of slower (summarized in Reynolds, 1988a) of year-round Plank- metabolism and growth. In more nutrient-replete envi- tothrix dominance of exposed, continuously mixed hy- ronments, the principal stress is imposed by having to pertrophic polder lakes in the Netherlands (first de- operate on low or intermittent light doses. Survival scribed by Berger, 1975), of the sustained dominance prospects are enhanced by motility, combined with in- of nanoplankton in the continuously flushed, ground- creased size, but the selective advantages of a high sur- water-flushed Montezuma’s Well in Arizona (Boucher face-to-volume ratio are not abandoned—the morpho- et al., 1984), and the unique dominance by Chlorella of logical attenuation among the acclimating R-type a cooling gradient across the hot-spring fed Rotowhero, diatoms and Planktothrix-type filaments offers a high New Zealand (Jolly and Brown, 1975). No less impres- tolerance of mechanical disturbance and the resilience sive is the striking commonality of the autopoetic orga- to recover from severe forcing events. nization of vertically segregated layers (or ‘‘plates’’) of The organizational trends imposed by disturbance algal and microbial producers on the stable physico- and stress press the selective bias toward the R or S chemical gradients in permanently ice-covered lakes in apices of the triangular template, shown in Fig. 5A. We Antarctica (e.g., Vincent, 1981), in tropical forest lakes have already seen that seasonal trends track through (Reynolds et al., 1983), and in midlatitude karstic do- the template matrix in broad, predictable ways (summa- lines (Vicente and Miracle, 1988). rized as S-ward and R-ward trends in Fig. 5B), but In contrast, however, the great majority of assem-

FIGURE 5 (A) From a starting condition, near the top left (C) corner of the triangle, environmental change moves to select increasingly for (S-) species tolerant of resource stress or for (R-) species tolerant of energy limitation (processing constraints); (B) major environmental restructuring alters the trajectory, changing the selection significantly; (C) under more frequent and perhaps less severe forcing, trajectories are redirected erratically, delaying progress to the competitive exclusion signified by the R and S apices. 594 PLANKTON, STATUS AND ROLE OF blages that have been sampled, identified, and described tropical forests, which in some ways, posed analogous in the literature are, simply, weakly organized. There questions to those raised by Hutchinson (1961) about need not be any paradox in this, once it is appreciated the plankton. The essence of Connell’s hypothesis is that in such accumulating, mid-successional assem- that frequent disturbance excludes all but fast-maturing blages most of the specific populations are not in any species; very infrequent disturbance allows competitive steady state but rather in a state of flux, either increasing exclusion to reduce diversity; therefore, maximum di- or decreasing in response to events in the recent past. versity is maintained at intermediate frequencies. Re- Thus, most so-called communities, in fact, comprise cently, this simply stated insight has been the subject populations which, at the given point in time, are in of a belated debate among ecologists. Setting aside those some stage between being dismantled and reassembled. who contest whether others had not put forward the The crucial questions about local diversity in the idea before Connell distilled it so elegantly and those plankton should be ‘‘How long has it been since a re- who complain (mistakenly) of a lack of experimental structuring was initiated by external forcing of a magni- evidence, the main line of argument has sought to dis- tude sufficient to create a disturbance?’’ and ‘‘At what tinguish the effects of disturbance intensity and of dis- rate is the restructuring taking place?’’ The field-scale turbance frequency. The debate is partly resolved by experiments carried out in the large limnetic enclosures recalling the fact that disturbance is solely the response in Blelham Tarn, England, pointed to a progress to to an imposed forcing. The reference point of whether steady-state monocultural dominance requiring from a disturbance has occurred at all and, if so, how intense 12 to 16 generations of the eventual dominant (Reyn- it was, should be most usefully found in comparison olds, 1988a). The time required for this could be as of the forcing energy and the accumulated cushioning few as 35 to 60 days, provided growth rates could be of the exergy flux. If structure has to be lost and re- sustained by water temperatures Ն20ЊC and a supply grouped as a consequence of an external force and if of carbon and nutrients of a capacity to support the the recovery depends on the restoration of opportunity, last population doubling. Accordingly, limitations on local Shannon diversity can be shown consistently to growth rate imposed by low temperature, slow carbon benefit during the reconstruction phase, when competi- renewal, or nutrient depletion extend the generation tion is least. At both high and low frequencies of forcing, times reciprocally, delaying the onset of the climactic the numbers of intermediate species are reduced so condition and slowing the exclusion of diversity. More that the inocula are no longer readily available to take likely, the intervention of external forcing (strong advantage of conditions under which their growth winds, heavy rain) would interrupt the successional might be favored. In contrast, local stocks of mid-suc- maturation at an earlier date, and if of sufficient magni- cessional species are enhanced by the sorts of opportu- tude (exceeding the net structural exergy flux), select- nities that might be provided every two or three genera- ing for alternative species with a new target outcome. tions by the (intermediate) rejuvenation of appropriate It was found consistently that the community response, growing conditions and with a marked alleviation of represented by two to four divisions of the newly se- severe interspecific competition in the early post-distur- lected species simultaneously with the dieback of the bance sequel. erstwhile-selected species, took some 5 to 15 days be- fore it was clearly manifest. It was deduced that a distur- bance frequency of this magnitude (two to four genera- B. Species Richness among Habitats tions) is sufficient to maintain an optimal local species It can be seen that the species representation contribut- diversity (Reynolds, 1988a). ing the local diversity remains heavily biased toward Analyses of temporal diversity fluctuations in small those that have been well represented in the recent past, lakes in locations as far apart as Canada (Trimbee and and which, of those whose growth should be favored Harris, 1983) and central Hungary (Padisa´k, 1993) con- by the onset of the appropriate environmental charac- firm the validity of this deduction, showing diversities teristics, remain potentially capable of seeding the in phytoplankton composition peaking within 11 days largest inocula from standing stocks of vegetative cells of a recognized physical stimulus. These and numerous and resting propagules. With the same kinds of environ- other case studies have been brought together to dem- mental variability affecting Shannon-type species diver- onstrate this planktonic validation of Connell’s (1978) sity in each tangible locality, there is still no clear expla- intermediate disturbance hypothesis (Padisa´k et al., nation as to why the collective representation of 1993). Its articulation followed from a consideration of planktonic organisms is so relatively species rich. We the celebrated diversity recognized in coral reefs and need a proposition for separate species representation PLANKTON, STATUS AND ROLE OF 595 in separated localities which recognizes that communi- for maintaining diversity in seasonally fluctuating envi- cation between localities is sufficient to maintain the ronments. high level of apparent cosmopolitanism among plank- In many cases, the propagules facilitate spatial trans- tonic organisms. In other words, we need to be aware fers as well. Dispersal in water droplets, or in dust, or of the roles of perennation and dispersal in relation to in or on the bodies of animals have been shown to be the maintenance of biodiversity. effective pathways of planktonic organisms (review of The survival of any species whose range of habitat Kristiansen, 1996) and to have been directly implicated suitability (as defined in section II) is discontinuous, in the establishment of populations in new or isolated in time as well as space, involves the separate develop- bodies of water (Maguire, 1963, 1977). Planktonic spe- ment of separated populations, but with a measure of cies are not equally amenable to dispersal, the trait being regenerative connection and gene renewal that resists related to other aspects of the life-history strategies; their permanent divergence. The metapopulation ecol- for instance, effective perennation and dispersion are ogy of plankton is not, formally, a well-rehearsed topic, essential properties of species of temporary or tempo- though there have been numerous studies to contribute rally variable habitats. In general, the dispersability, or a general appreciation of the principles. Although the invasiveness, of propagules (or, indeed, of vegetative existence of liquid water on the planet has a very long cells) is dependent on a raft of such species-specific geological history, individual bodies of fresh waters are features as their sizes, their resistance to desiccation, extremely transient. With the exception of the basins and the numbers and frequencies with which they are formed by tectonic movements, a majority of these is produced. The probability (p) of a given species (A) less than 20,000 years in age. The idea of lakes as islands being able to establish itself in another water body will in a terrestrial sea is an easy one to assimilate, even if be determined as a function, partly of its relevant spe- we wish to extend the analogy to suggest they are like cies-specific traits (TA) and partly of the problems posed volcanic eruptions that are shortly to be eroded back to all would-be invaders of the distance (d) and size under the sea. The actual oceans are physically and (a) of the new (or ‘‘target’’) site from the existing (or temporally contiguous, but the patterns of global circu- ‘‘source’’: MacArthur and Wilson, 1967) population: lation allow significant habitat differentiation to be maintained at the scales at which planktonic organisms live their lives. The principles of island biogeography propounded by MacArthur and Wilson (1967) provide a good model for plankton ecology. An important converse of this relationship also mani- The temporal discontinuities are most appropriately fests itself in relation to the ongoing suitability or effec- bridged by the production of resistant, resting propa- tiveness of source and target sites as a habitat for the gules. Even the most elementary biological texts on given species. Either because the habitat changes in aquatic protists are memorably punctuated with refer- consequence of autogenic properties or because species ences to the production ‘‘of cysts, to survive adverse A is prevented from completing its perennation in that conditions.’’ Certainly, among the freshwater phyto- habitat, through the intervention of a facultative preda- plankton, almost all the major groups represented pro- tor or pathogen, it is ultimately likely that the survival duce some kind of physiological resting stage, if not a of the species in that location is at risk. Repeated at discrete resting spore, cyst or akinete, some of which several sites, this process would threaten the survival can remain dormant for many years and still be fully of the species in its entirety and bring about a diminu- viable (see Reynolds, 1984a; over 60 years in the case tion in total species richness (i.e., the biodiversity). The of some Anabaena akinetes in a dated lake sediment). resistance to that comes, quite literally, from the patch Eggs may fulfill a similar role for zooplankton, main- dynamics of habitat distribution and their temporal taining banks of inocula, pending the restoration of suitability to species A. Thus, the status of species A is conditions favorable to growth and recruitment of suc- a function of the number of possible habitat patches cessive generations (Hairston, 1996). Produced in ade- (N), the number that is occupied (O), the rate at which quate numbers, such dormant life-history stages pro- they become excluded therefrom (e), and the probabil- vide a significant survival ‘‘hedge’’ through periods of ity (p) of colonizing the (N-O) unoccupied habitats. hostile conditions (low temperature, low light, poor The rate of expansion (or loss) of the metapopulation resources or food availability, drought, and so on). The in time (dO/dt) may the be symbolized: inocula potentially supplied by subsequent spore germi- nation and egg hatching provide a powerful mechanism 596 PLANKTON, STATUS AND ROLE OF

For the more familiar and (supposedly) more cosmo- This last distinction permits the differentiation of politan planktonic forms, relative ease of dispersal is, invasive and accumulative life-history strategies. They manifestly, the dominant factor upholding the wide- have equal merit because they exploit different frequen- spread occupancy among suitable habitats. For the ma- cies and intensities of environmental fluctuation. In- jority of known species that are relatively rare (that is, deed, the full range of conservative mechanisms may be there is a relatively low occupancy among the total considered to have evolved to maximize the exploitative number of patches), effective dispersal may be resisted opportunities provided by the variability within and by specific traits (TA) or simply by low numbers. In between the available habitats. Consequently and con- this case, survival may be considered more tenuous. versely, it is the variety of dimensions and scales of However, from the limited investigative evidence avail- variability that upholds the diversity of species. The able, many of these rarer species have been numerous in nearest that we can get to a short answer to the biodiver- the past and occasionally continue to perform relatively sity question is that it is the means by which living well on the inertia of persistent, viable propagules. systems cope with a nonequilibrium world. While the length of this ‘‘ecological memory’’ (Padisa´k, The feature distinguishing plankton-based ecosys- 1992) is not certainly quantified, we may be aware of tems from terrestrial ones is that the relevant temporal the fact that it is generally the rarer species that contrib- scales are mostly much shorter in open waters than on ute most to the total biodiversity of planktonic organ- the land. Not only are the mechanisms of planktonic isms. Whereas the metabolically significant planktonic biodiversity conveniently observed but, provided that biomass relies on the productivity of a relatively small appropriate scaling factors are applied, the study of number of species in a series of variable and renewable planktonic systems may be rewarded with insights into habitats, the majority of species is limited to habitats current issues about the importance and the protection in which temporal variability is less extreme or exclu- of biodiversity. sion is long protracted. Of the many propositions that have been advanced about the role of diversity in upholding ecosystem pro- cesses, current attention focuses mainly on four broad postulates (Lawton, 1997). In various ways, they relate VIII. CONCLUSIONS AND to Darwin’s (1859) proposition that a large number of IMPLICATIONS species imparts a higher level of functional stability than does a small one. Thus, to lose species inevitably There is scarcely a short answer to the question, impairs the functional integrity of the ecosystem. The ‘‘How is biodiversity maintained in the plankton?’’ ‘‘redundant species hypothesis’’ counters that, because The available evidence is that there is an operative species are not equally represented, some are contribut- blend of those mechanisms hypothesized to underpin ing much more than others to ecosystem function. In- diversity in other ecosystems. Global species richness deed, some ‘‘keystone species’’ (Paine, 1969) drive the is assisted by protracted isolation of populations and main functions and have a much stronger influence endemism of subsequently differentiated species to than ‘‘passenger’’ species (Walker, 1992). Then, logic such locations as Lake Baykal and small lakes in suggests, a minimal diversity is essential to adequate Australasia. Progressive functional adaptations and ecosystem functioning and most of the species are really niche specialism among, for example, the photobacte- redundant in their roles (Lawton and Brown, 1993; ria, the cyanoprokaryotes, and the planktonic crusta- Walker, 1992). Almost diametrically opposed to this cea contribute to the pervasion of selected species view is the ‘‘rivet hypothesis’’ (Ehrlich and Ehrlich, into sites offering their preferred habitat conditions 1981), which accords to each species an essential con- for long time periods, even when those sites are tributory role, and which, if lost from the whole, like sometimes mutually remote. However, the majority rivets lost from the structure of an aircraft, quickly lead of species seem to be reliant on the periodic rejuvena- to serious functional impairment and failure. A third tion of a broad range of habitat conditions and the hypothesis takes a much looser view, suggesting that opportunity to fill, mainly noncompetitively, the spare function is modified by changes in the richness of spe- capacity that is thus regenerated. On the basis that cies composition but in unpredictable ways (‘‘idiosyn- opportunities are simultaneously closing, there is an cratic’’; Lawton, 1994) because the contributions of in- implicit dependence on the maintenance of viable dividual species to system function are unequal. The seed banks and the ability to combine this either fourth possibility is the null hypothesis that ecosystems with efficient dispersal or with high survivorship. are insensitive to changes in species composition. This PLANKTON, STATUS AND ROLE OF 597 seems increasingly to be implausible and will not be ocean circulation is but a piece in the biospheric mosaic. discussed. The essential general aim should be to ensure that suit- One of the important lessons from the plankton scale able habitat elements persist, each in a range of develop- is that a distinction should be made between structural mental states. Local extinctions are resisted by good stability and functional stability. Taking the basic func- between-locality communication of propagules. In this tion of the plankton to be the material cycling of matter sense, managing biodiversity has to adopt the philoso- in open water, driven by solar energy invested in carbon phies of patch dynamics, taking full account of the bonds, the photoautotrophic, heterotrophic and phago- longevities and the invasiveness of species-specific pop- trophic roles are fulfilled, respectively, by any or all of ulations in relation to the externally influenced avail- a large number of species of phytoplankton, bacteri- ability and renewal of suitable patches. oplankton, and zooplankton. Despite having vastly dif- ferent and frequently changing species compositions, studies of the productivity of planktonic systems dem- See Also the Following Articles onstrate a remarkable level of functional coherence (Schindler, 1990). In this way, pelagic fish may con- BACTERIAL BIODIVERSITY • ESTUARINE ECOSYSTEMS • LAKE • • tinue to feed planktivorously and to respire photosyn- AND POND ECOSYSTEMS OCEAN ECOSYSTEMS REEF ECOSYSTEMS • RIVER ECOSYSTEMS thetically generated oxygen almost without reference to the planktonic structure, just so long as similar func- tions are maintained. At the level of planktonic communities, a decline in Bibliography the population of a dominant species will carry fewer Atlas, R. M., and Bartha, R. (1993). Microbial Ecology—Fundamentals implications if a second species is poised to substitute and applications. 3rd ed. Benjamin Cummings, Redwood City. quickly. Frost et al. (1995) made the case that species Azam, F., Fenchel, T., Field, J. G., Gray, J. 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