GRASSES AND GRASSLAND ECOLOGY This page intentionally left blank Grasses and Grassland Ecology
David J. Gibson Southern Illinois University, Carbondale
1 3 Great Clarendon Street, Oxford OX2 6DP Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offi ces in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York © Oxford University Press 2009 The moral rights of the author have been asserted Database right Oxford University Press (maker) First published 2009 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Data available Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India Printed in Great Britain on acid-free paper by CPI Antony Rowe, Chippenham, Wiltshire
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10 9 8 7 6 5 4 3 2 1 Preface
. . . a vast expanse of level ground unbroken save by one My own experience in grasslands results from thin line of trees which scarcely amounted to a scratch an early and abiding love of the chalk grasslands upon the great blank; until it met the glowing sky of southern England. The dune grasslands of wherein it seemed to dip . . . There it lay, a tranquil sea Newborough Warren, Anglesey and the montane or lake without water . . . with the day going down upon grasslands of Snowdonia, Wales have also been it . . . it was lovely and wild, but oppressive in its barren important to me ever since my days as a doctoral monotony. student at the University College of North Wales Charles Dickens (American Notes for General Circulation, (now the University of Bangor). My research in 1842) describing Looking Glass Prairie grasslands has been inspired by many mentors and near Lebanon, Illinois colleagues, but I must mention in particular Paul Risser (formerly of the University of Oklahoma), Grasslands evoke emotion, they are the largest the late Lloyd Hulbert (Kansas State University), biome on Earth, they represent a tremendous source and the Long Term Ecological Research group at of biodiversity, they provide important goods and Konza Prairie during the late 1980s as having a services, and they are the place where as a species, large and enduring influence on my understand- we first stood up and walked. As a result, grasses ing of the North American prairie. The writing of and grasslands are widely studied. However, after this book follows from the start that they gave me. teaching an upper level/postgraduate course on It takes a long time to write a book, but I am grassland ecology for several years, I realized that a grateful to Southern Illinois University Carbondale suitable textbook was needed. Hence, I have written for providing a sabbatical leave in Spring 2006 this book in the hope that it will be useful not just that allowed time to write several chapters. Many, for the students taking my grassland course, but many people helped me write this book. In par- researchers, land managers, and anyone who has ticular, I thank colleagues who answered my an interest in grasslands anywhere in the world. questions and read drafts of various chapters The book brings together a huge literature from including Roger Anderson (Chapter 10), Elizabeth ecological, natural history, and agricultural disci- Bach (Chapter 1), Sara Baer (Chapters 7 and 10), plines. The nomenclature for plant names is syno- Ray Callaway (Chapter 6), Ryan Campbell (Index), nymized according to the USDA Plants National Gregg Cheplick (Chapter 5), Keith Clay (Chapter Database (http://plants.usda.gov/index.html) as 5), Jim Detling (Chapter 9), Stephen Ebbs (Chapter of May 2008, or, for species not in the database, 4), Don Faber-Langendoen (Chapter 8), Richard the name used in the original source. As a result, Groves (Chapter 8), Trevor Hodkinson (Chapter 2), names are changed from the original source when a Allison Lambert (Chapters 1, 2, 3, 4, and 8), Susana more up-to-date name is provided in the database. Perelman (Chapter 8), Wayne Polley (Chapter 4), Some familiar plants have new names: for exam- David Pyke (Chapter 10), Steve Renvoize (Chapter ple, where I talk about tall fescue I use Schedonorus 3), Paul Risser (Chapter 1), Tim Seastedt (Chapter 7), phoenix in place of the older Festuca arundinacea. Rob Soreng (Chapter 2), and Dale Vitt (Chapter 8). Older names are included in the index with a ref- Thanks to Daniel Nickrent, Hongyan Liu, Gervasio erence to the new name. Piñeiro, Sam NcNaughton, Dale Vitt, Steve Wilson,
v vi PREFACE and Zicheng Yu for allowing me to reproduce their tirelessly helpful in ensuring that this book was excellent photographs. John Briggs kindly supplied actually published. Finally, grateful thanks to my the satellite image for Plate 13 and Howard Epstein wife Lisa and our children Lacey and Dylan for an original for Fig 4.3. Cheryl Broadie and Steve providing the love and emotional support neces- Mueller of the SIUC IMAGE facility were a tremen- sary for the marathon of writing a book. dous help in preparing several of the photographs Carbondale, Illinois D.J.G and figures. Helen Eaton, Ian Sherman, and the May 2008 staff at Oxford University Press have always been Contents
Preface v
1 Introduction 1 1.1 Grasslands: a tautological problem of defi nition 1 1.2 Extent of the world’s grasslands 2 1.3 Grassland loss 4 1.4 Grassland goods and services 12 1.5 Early grassland ecologists 18
2 Systematics and evolution 21 2.1 Characteristics of the Poaceae 21 2.2 Traditional vs modern views of grass classifi cation 22 2.3 Subfamily characteristics 24 2.4 Fossil history and evolution 29
3 Ecological morphology and anatomy 35 3.1 Developmental morphology—the phytomer 35 3.2 Structure of the common oat Avena sativa 36 3.3 Culms 36 3.4 Leaves 43 3.5 Roots 46 3.6 Infl orescence and the spikelet 49 3.7 The grass seed and seedling development 51 3.8 Anatomy 54
4 Physiology 58
4.1 C3 and C4 photosynthesis 58 4.2 Forage quality 68 4.3 Secondary compounds: anti-herbivore defences and allelochemicals 73 4.4 Silicon 78 4.5 Physiological integration of clonal grasses and mechanisms of ramet regulation 79
5 Population ecology 81 5.1 Reproduction and population dynamics 81 5.2 Fungal relationships 94 5.3 Genecology 102
vii viii CONTENTS
6 Community ecology 110 6.1 Vegetation–environment relationships 110 6.2 Succession 113 6.3 Species interactions 115 6.4 Models of grassland community structure 121 6.5 Summary: an issue of scale 128
7 Ecosystem ecology 129 7.1 Energy and productivity 129 7.2 Nutrient cycling 141 7.3 Decomposition 149 7.4 Grassland soils 153
8 World grasslands 160 8.1 Ways of describing vegetation 160 8.2 General description of world grasslands 162 8.3 Examples of regional grassland classifi cations 179
9 Disturbance 184 9.1 The concept of disturbance 185 9.2 Fire 187 9.3 Herbivory 194 9.4 Drought 207
10 Management and restoration 211 10.1 Management techniques and goals 211 10.2 Range assessment 221 10.3 Restoration 235
References 243 Plant index 289 Animal index 297 Subject index 299 CHAPTER 1 Introduction
Each grass-covered hillside is an open book for those The main points that these varied definitions have who care to read. Upon its pages are written the condi- in common are the prevalence of grasses (members tions of the present, the events of the past, and a forecast of the Poaceae), an infrequent or a low abundance of those of the future. Some see without understand- of woody vegetation, and a generally arid climate. ing; but let us look closely and understandingly, and act Risser’s (1988) definition is perhaps the most com- wisely, and in time bring our methods of land use and prehensive as it encompasses these ideas. Other conservation activities into close harmony with the dic- factors that are important and which together help tates of Nature. characterize natural grasslands in many parts of John E. Weaver (1954) the world include deep, fertile, organic-rich soils (frequently Chernozems—see Chapter 7), frequent The purpose of this first chapter is to introduce the natural fire (Chapter 9), and large herds of graz- grassland biome. Grasslands are the most extensive, ing mammals (Chapter 9). Semi-natural or seeded arguably the most useful to human society, yet the grasslands (e.g. amenity grasslands: Chapter 8) most threatened biome on the planet. Nevertheless, may lack some of these features, especially natural it is surprisingly difficult to unambiguously define disturbance. grassland. Here we seek such a definition (§ 1.1); As with most disciplines there is a series of discuss where grasslands occur (§ 1.2); how they terms, almost a language, relating specifically to are being lost, fragmented, and degraded (§ 1.3); grasslands (Table 1.2). A number of these terms and summarize their outstanding and immense have their origin in a long history of grassland value (§ 1.4). The chapter finishes with a brief biog- management for grazing, i.e. range management raphy of John Bews and John Weaver, two of the (Chapter 10). Many of these terms have become early pioneers of grassland ecology (§ 1.5). formalized by the appropriate professional organ- izations, e.g. the Forage and Grazing Terminology Committee representing more than half a dozen 1.1 Grasslands: a tautological problem agencies and societies from the USA, Australia, of definition and New Zealand. Several of the terms listed in At its simplest, grassland can be defined as ‘a habi- Table 1.2 are often used synonymously (e.g. prairie tat dominated by grasses’, however a more useful, and grassland in the North American Midwest), strict, but all-encompassing definition is elusive but others refer specifically to a particular type (Table 1.1). Indeed, many authorities do not pro- of grassland (e.g. savannah) or geographic loca- vide a definition, assuming merely that we know a tion (e.g. veld, spinifex). The distinction between grassland when we see one. Others prefer to define meadow and pasture, reflecting their use and a grassland by the absence of specific features; for management through mowing and grazing respec- example, Milner and Hughes (1968) offered a flor istic tively, goes back hundreds of years and is reflected definition (Table 1.1), but added that a more useful in several European languages; e.g. French pré and approach is to consider grassland physiognom- prairie, German Wiese and Weide, and the Latin pra- ically or structurally as ‘a plant community with tum and pascuum (Rackham 1986). Terms such as a low-growing plant cover of non-woody species.’ forage and herbage refer specifically to the fraction
1 2 GRASSES AND GRASSLAND ECOLOGY
Table 1.1 Grassland defi nitions
Definition Source
‘. . . the great empty middle of our continent . . . is indivisible. It endures . . . aridity is the first defining Manning (1995) and implacable factor . . . a place of journeys . . . treeless plains . . . ‘ ‘. . . a plant community in which the Gramineae are dominants and trees absent.’ Milner and Hughes (1968) ‘. . . a vegetation type dominated by grasses but containing many broadleaf herbs (forbs).’ Bazzaz and Parrish (1982) ‘Land on which the vegetation is dominated by grasses.’ The Forage and Grazing Terminology Committee (1992) ‘A general lack of woody vegetation helps define grasslands . . . ‘ Knapp and Seastedt (1998) ‘[grasslands] . . . are dominated primarily by grasses (Gramineae) and grass-like plants (mostly Sims (1988) Cyperaceae) . . . climates generally have distinct wet and dry seasons and are noted for temperature and precipitation extremes.’ ‘. . . terrestrial ecosystems dominated by herbaceous and shrub vegetation, and maintained by fire, Pilot Assessment of Global grazing, drought and/or freezing temperatures.’ Ecosystems; White et al. (2000). ‘One-fourth or more of the total vegetation consists of primarily herbaceous communities in which Kucera (1981) the Gramineae are the dominant life form . . . the grasses give character and unity of vegetal structure to the landscape . . . . an overstory of scattered trees and shrubs may be present.’ ‘ . . . any plant community, including harvested forages, in which grasses and/or legumes make up the Barnes and Nelson (2003) dominant vegetation.’ ‘A region with sufficient average annual precipitation (25–75 cm [10–30 inches]) to support grass Stiling (1999) but not trees.’ ‘<1 tree per 5 acres . . . on slopes of 2–4%’ Anderson (1991) ‘. . . types of vegetation that are subject to periodic drought, that have a canopy dominated by grass Risser (1988) and grasslike species, and that grow where there are fewer than 10 to 15 trees per hectare.’
of grassland useful to the range manager. Forage is widely accepted account, estimates grasslands as a particularly relevant and important component covering 52 544 000 km2 or 40.5% of the total land since it defines the portion used as feed for domes- area (White et al. 2000; World Resources 2000–2001). tic herbivores. Forage science is a specialized agri- The PAGE Classification of grasslands excludes cultural discipline in its own right (e.g. Barnes et al. urban areas as defined by the Nighttime Lights 2003). Overall, the terms and language associated of the World Database (estimated at 1010 km2) with grasslands reflect both what these ecosystems but is nevertheless broad, including savannahs have in common and their diversity related to an (17.9 106 km2), open and closed shrublands extensive, worldwide distribution. (16.5 106 km2), and tundra (7.4 106 km2), as well as non-woody grasslands (10.7 106 km2). T he PAGE 1.2 Extent of the world’s grasslands classification is based on satellite imagery of land cover from the International Geosphere-Biosphere Globally, grasslands occur on every continent Programme Data and Information System (IGBP- (excluding Antarctica) occupying 41–56 106 km2, DIS) DISCover 1 km resolution land cover maps covering 31–43% of the earth’s surface (World obtained using the Advanced Very High Resolution Resources 2000–2001, and references therein) Radiometer (AVHRR) data (Loveland et al. 2000). (Plate 1). This range in estimates reflects differences Under the PAGE classification, grasslands in defining grassland by different authorities, par- occupy more of the earth’s surface than the other ticularly in the extent to which cropland, tundra, major cover types, i.e. forests (28.97 106 km2) or or shrublands are included. The Pilot Analysis of agriculture (36.23 106 km2) (White et al. 2000). Global Ecosystems (PAGE) Classification, the most Nearly 800 106 people live throughout this large INTRODUCTION 3
Table 1.2 Grassland terminology (source indicated where appropriate). The defi nitions reproduced here from Thomas (1980) are derived and modifi ed from those also provided by Hodgson (1979)
Term Definition Source
Forage Any plant material, including herbage but excluding concentrates, used as feed for (Thomas 1980) domestic herbivore Herbage The above-ground parts of a sward viewed as an accumulation of plant material (Thomas 1980) with characteristics of mass and nutritive value Meadow A tract of grassland where productivity of indigenous or introduced forage is (Forage and Grazing modified due to characteristics of the landscape position or hydrology, e.g. hay Terminology Committee 1992) meadow, wet meadow Pasture A type of grazing management unit enclosed and separated from other areas by (Forage and Grazing fencing or other barriers and devoted to the production of forage for harvest Terminology Committee 1992) primarily by grazing Pastureland Land devoted to the production of indigenous or introduced forage for harvest (Forage and Grazing primarily by grazing. Terminology Committee 1992) Permanent pasture Pastureland composed of perennial or self-seeding annual plants that are grazed (Barnes and Nelson 2003) annually, generally for 10 or more successive years Prairie French term for grassland, used now to describe the grasslands of the North (Forage and Grazing American Great Plains. Defined in the USA as nearly level or rolling grassland, Terminology Committee 1992) originally treeless, and usually characterized by fertile soil Rangeland American term for land on which the indigenous vegetation is predominantly (Forage and Grazing grasses, grass-like plants, forbs, or shrubs and is managed as a natural ecosystem Terminology Committee 1992) Sod A piece of turf dug up, or pulled up by grazing animals (ThomasF 1980) Savannah Grassland with scattered trees or shrubs; often a transitional type between true (Forage and Grazing grassland and forestland and accompanied by a climate with alternating wet and Terminology Committee 1992) dry seasons Spinifex Australian steppe area dominated by the grass spinifex (Triodia spp.) with (Skerman and Riveros 1990) occasional shrubs (Acacia spp.) and low trees (Eucalyptus spp.) Steppe Semi-arid grassland characterized by short grasses occurring in scattered bunches (Forage and Grazing with other herbaceous vegetation and occasional woody species. Terminology Committee 1992) Sward An area of grassland with a short (say <1 m tall) continuous foliage cover, including (Thomas 1980) both above-ground and below-ground plant parts but excluding any woody plants. Veld Afrikaans term for South African grassland with scattered trees of shrubs Bews (1918)
area, more than the number in forests (c.450 106 Oceania (including New Zealand and Australia) at people), but less than those in agricultural areas 6000–7000 106 km2 each (Table 1.3). On an area (2.8 109 people: 1995 estimates). Most of the basis, 11 countries across the globe have each in 800 106 grassland inhabitants live in savan- excess of 1 106 km2 of grassland area, with the nah regions (413 106), and within the savannah top country being Australia with 6.6 106 km2 region the majority (266 106) are in sub-Saharan (Table 1.4). It is notable that each of the major Africa (White et al. 2000). By contrast, the least regions of the world is represented in this list. On populated grassland region is the tundra (11 106) a percentage area basis, 11 countries have 80% and within that only 104 000 people live in North of their area under grassland (Table 1.5), with American tundra grasslands. Benin having the largest percentage at 93.1%. Of Across the globe, grasslands are most extensive these countries, 9 are in sub-Saharan Africa, and in sub-Saharan Africa (14.46 106 km2) followed by all are quite small with less than 1 106 km2 land Asia (excluding the Middle East) at 8.89 106 km2, area (Mozambique is the largest at 825 606 km2). and the grasslands of Europe, North America, and Australia, with the largest expanse of grassland of 4 GRASSES AND GRASSLAND ECOLOGY
Table 1.3 Grassland area (km2 106) and population in world regions, excluding Greenland and Antarctica. Adapted from White et al. (2000)
Region Savannah Shrubland Non-woody Tundra Global Population grassland grassland (000)
Asiaa 0.90 3.76 4.03 0.21 8.89 249 771 Europe 1.83 0.49 0.70 3.93 6.96 20 821 Middle East and North Africa 0.17 2.11 0.57 0.02 2.87 110 725 Sub-Saharan Africa 10.33 2.35 1.79 0.00 14.46 312 170 North America 0.32 2.02 1.22 3.02 6.58 6 125 Central America and Caribbean 0.30 0.44 0.30 0.00 1.05 30 347 South America 1.57 1.40 1.63 0.26 4.87 56 347 Oceania 2.45 3.91 0.50 0.00 6.86 3 761 World 17.87 16.48 10.74 7.44 52.53 789 992
a Excluding Middle Eastern countries.
Table 1.4 Top countries for grassland area (countries with >1 000 000 km2 of grassland)
Country Regiona Total land area Total grassland (km2) area (km2)
Australia Oceania 7 704 716 6 576 417 Russian Federation Europe 16 851 600 6 256 518 China Asia 9 336 856 3 919 452 United States North America 9 453 224 3 384 086 Canada North America 9 908 913 3 167 559 Kazakhstan Asia 2 715 317 1 670 581 Brazil South America 8 506 268 1 528 305 Argentina South America 2 781 237 1 462 884 Mongolia Asia 1 558 853 1 307 746 Sudan Sub-Saharan Africa 2 490 706 1 292 163 Angola Sub-Saharan Africa 1 252 365 1 000 087
a Asia excludes Middle Eastern countries. From White et al. (2000).
any country, has the sixth highest percentage land Orange, Limpopo, Mangoky, and Mania, of which area under grassland (85.4%). 13 are in Africa, 5 in Asia, 3 in South America, 2 Grasslands contribute ecosystem functions to in North America, 1 shared between North and many of the world’s major watersheds; i.e. water Central America, and 1 in Oceania (Fig. 1.1). None catchment areas that provide a functional unit of of the mapped watersheds in Europe had more the landscape. A survey of 145 mapped watersheds than 25% grassland. representing 55% of the world’s land area (exclud- ing Greenland and Antarctica) showed 25 water- 1.3 Grassland loss sheds possessing 50% grassland cover. These watersheds include the Senegal, Niger, Volta, Nile, Covering such a large area of the earth’s land sur- Turkana, Shaballe, Jubba, Zambezi, Okavango, face, it is no surprise that grasslands have been INTRODUCTION 5
Table 1.5 Top countries for percentage of grassland area (countries with >80% grassland area)
Country Regiona Total land Grassland International tourists International tourist area (km2) area (%) (000 yr −1) (±% 10 yr receipts (million US$ change)b yr −1) (±10 yr change)b
Benin Sub-Saharan Africa 116 689 93.1 145 (+150) 28 (–7) Central African Republic Sub-Saharan Africa 621 192 89.2 23 (+331) 5 (–6) Botswana Sub-Saharan Africa 579 948 87.8 693 (+160) 174 (+361) Togo Sub-Saharan Africa 57 386 87.2 ND ND Somalia Sub-Saharan Africa 639 004 86.7 10 (–74) ND Australia Oceania 7 704 716 85.4 4059 (+180) 8503 (+471) Burkina Faso Sub-Saharan Africa 273 320 84.7 693 (+160) 32 (+459) Mongolia Asia 1 558 853 83.9 87 (–57) 21 (ND) Guinea Sub-Saharan Africa 246 104 83.5 96 (ND) 4 (ND) Mozambique Sub-Saharan Africa 788 938 81.6 ND ND Namibia Sub-Saharan Africa 825 606 80.6 405 (ND) 214 (ND) a Asia excludes Middle East countries. b Change from 1985–1987 to 1995–1997. ND, no available data. From White et al. (2000)
Indigirka Syr Darya Lake Balkhash Brazos Colorado Amu Darya Yellow Rio Grande Niger Nile Shaballe Senegal Jubba Lakes Titicaca & Salar de Uyuni Volta Lake Turkana Zambezi Okavango Maria Watersheds with Orange Murray >50% grassland Mangoky area Rio Limpopo Colorado Chubut
Figure 1.1 Grassland watersheds of the world. With permission from White et al. (2000).
heavily used throughout human history. For exam- 9000 years (Gillison 1992). Indeed, it is widely held ple, in Australia, a close interaction between humans that Homo sapiens may have arisen in the savan- and grassland fire is though to have existed for nahs of Africa (Stringer 2003). Further back, grass- 40 000 years or more (Gillison 1992). In Papua New lands are associated with the co-evolution of major Guinea, a similar relationship with slash-and-burn plant and animal groups—the grasses and grazing agriculture is thought to have existed for at least mammals, respectively (Chapter 2). 6 GRASSES AND GRASSLAND ECOLOGY
Grasslands have been lived in and used by that habitat conversion exceeds protection in grass- people throughout human history. Inevitably this lands more than in any other terrestrial biome; has led to tremendous changes, and most recently only 1 ha of grassland is protected for every 10 ha the loss of much of this biome. The major modifica- lost. The Conservation Science Program–World tions to grassland cover are due to: Wildlife Fund–US Global 200 programme identi- fied 17 grassland ecoregions worldwide that are ● agriculture ‘critically endangered’ (Table 1.7), with an addi- ● fragmentation tional 13 that are considered ‘vulnerable’ (Olson ● invasive non-native species and Dinerstein 2002). Ecoregions are fine-scale ● fire (lack of) regional ecological areas within a biome that are ● desertification characterized by local geography and climate ● urbanization/human settlements and a unique assemblages of species. The criti- ● domestic livestock. cally endangered and vulnerable grassland ecore- Of these, the first three—agriculture, fragmen- gions comprise some of the world’s most diverse tation, and non-native species—pose perhaps and spectacular grasslands, including, for exam- the greatest threat to native grasslands and are ple, the Terai–Duar savannahs and grasslands discussed below. The extent of urbanization is in southern Asia, which are alluvial grasslands reported in Table 1.6, desertification is discussed dominated by 7 m high Saccharum spp. (elephant in Chapter 8, and the effects of fire and domestic grass) and Asia’s highest density of tigers, rhinos, grazers are discussed in Chapters 9 and 10. and ungulates. Other critically endangered areas Globally, there has been large-scale conversion include the South African fynbos and south-west of grassland to human-dominated uses; of the Australian forests and scrub ecoregions, both of world’s 13 terrestrial biomes, 45.8% of temperate which include extensive grassy components and grasslands, savannahs and shrublands, 23.6% of harbour very high levels of diversity and ende- tropical/subtropical grasslands, savannahs, and mism. All of the critically endangered areas iden- shrublands, 26.6% of flooded grasslands and tified in the Global 200 programme are suffering savannahs, and 12.7% of montane grasslands and the effects of habitat loss and alteration. shrublands have been converted (Hoekstra et al. The greatest alteration to grasslands world- 2005). With only 4.6% of the habitat protected, wide has been through transformation to temperate grasslands, savannahs, and shrublands agricultural land creating in many places a have a higher Conservation Risk Index (ratio of grassland/agricultural mosaic, or in other areas habitat converted to habitat protected 10:1) than wholesale conversion to agriculture (Fig. 1.2). any of the other terrestrial biomes. This means The greatest loss of grassland area is in North
Table 1.6 Estimated remaining and converted grassland (%)
Continent and region Remaining in Converted to Converted to Total grasslands (%) croplands (%) urban areas (%) converted (%)
N. America: Tallgrass prairie in the United States 9.4 71.2 18.7 89.9 S. America: Cerrado woodland and savannah in Brazil, 21.0 71.0 5.0 76.0 Paraguay, and Bolivia Asia: Daurian steppe in Mongolia, Russia, and China 71.7 19.9 1.5 21.4 Africa: Central and eastern Mopan and Miombo in 73.3 19.1 0.4 19.5 Tanzania, Rwanda, Burundi, Dem. Rep. Congo, Zambia, Botswana, Zimbabwe and Mozambique Oceania: South-west Australian shrublands and 56.7 37.2 1.8 39.0 woodlands
From White et al. (2000). INTRODUCTION 7
America where only 9.4% of the original tallgrass remained by 1978 (Illinois Department of Energy prairie remains (Table 1.6). Locally the loss can and Natural Resources 1994). Ten other states have be even greater, as in the state of Illinois, where also reported declines of 90% in the extent of only 0.01% (9.5 km2) of high-quality native prairie tallgrass prairie. Globally, large areas of grassland
Table 1.7 Critically endangered grassland ecoregions
Major habitat Biogeographic realm Ecoregion
Tropical and subtropical grasslands, savannahs, and Afrotropical Sudanian savannahs shrublands Indo-Malayan Terai-Duar savannahs and grasslands Temperate grasslands, savannahs, and shrublands Nearctic Northern prairie Neotropical Patagonian steppe Flooded grasslands and savannahs Afrotropical Sudd-Sahelian flooded grasslands and savannahs Indo-Malayan Rann of Kutch flooded grasslands Neotropical Pantanal flooded savannahs Montane grasslands and shrublands Afrotropical Ethiopian highlands Southern rift montane woodlands Drakensberg montane shrublands and woodlands Mediterranean forests, woodlands, and scrub Afrotropical Fynbos Australasia South-western Australia forests and scrub Nearctic California chaparral and woodlands Neotropical Chilean matorral Palearctic Mediterranean forests, woodlands, and scrub Deserts and xeric shrublands Afrotropical Madagascar spiny thicket Australasia Carnavon xeric scrub
From Olson et al. (2000).
Grassland and agriculture mosaic Grassland Non-grassland area
Figure 1.2 The global grassland/agriculture mosaic. With permission from White et al. (2000). 8 GRASSES AND GRASSLAND ECOLOGY have also been converted to agriculture in South of numerous studies attest to these detrimental America and Oceania (21% and 56.7% remaining, affects (Saunders et al. 1991). For example, in Ohio respectively). In all areas, grassland loss is predom- grasslands, the upland sandpiper, bobolink, savan- inantly through conversion to cropland rather than nah sparrow, and Henslow’s sparrow, were found to urban areas. Excluding agricultural mosaics to be area-sensitive being encountered most fre- from remaining grasslands reduces global grass- quently only on grassland tracts 0.5 km2 (Swanson land area by c.7.1 106 km2, particularly in sub- 1996). Habitat fragmentation was found to disrupt Saharan Africa (3.5 106 km2) (White et al. 2000). plant–pollinator and predator–prey interactions in Substantial areas in South America (1.4 106 km2) central European calcareous grasslands (Steffan- and Asia (1.2 106 km2) have also been altered by Dewenter and Tscharntke 2002). In grasslands of agriculture (Fig. 1.2). the US Great Plains, intensive land use following Wholesale loss to cropland leads to immedi- grassland fragmentation was shown to provide ate loss of grassland, but fragmentation, in which hotspots for exotic birds (Seig et al. 1999). blocks of habitat are dissected into smaller units, Paradoxically, many conservationists in Europe can produce a more insidious and gradual decline lament the decline of managed semi-natural grass- in ecosystem structure and function. The extent land because many of these grasslands are spe- of grassland fragmentation was illustrated by cies-rich. By the end of last Ice Age (c.10 000 bc), White et al. (2000) who reported that 37% of 90 the British Isles were covered with forests, with grassland regions analysed in North America and grasslands being rare and restricted to a few Latin America occurred as small linear patches. In high- altitude montane areas (Pennington 1974). another analysis, they showed that road networks Extensive forest clearance and farming began in the Great Plains of the USA fragmented 70% of around 4000 bc and continued for centuries, into the prairie into patches of 1000 km2. The extent Roman times (Rackham 1986). Some of the earliest of grassland fragmentation can be deceptive at first written records of grassland use are recorded in the glance for without factoring in the road networks, it Domesday Book, William the Conqueror’s survey appeared that 90% of the grassland was composed of Britain dating from 1086. Mowed meadows were of blocks of 10 000 km2 or more. Globally, White the best-recorded land-use in Domesday, account- et al. (2000) estimated that nearly 37% of grasslands ing for 1.2% of the land area surveyed (c.1214 km2), are characterized by small and few habitat blocks, with pasture being mentioned more sporadi- high fragmentation, or both. cally. For example, in the Lindsey subcounty of In addition to affecting estimates of grassland Lincolnshire, 178 km2 of meadow were recorded, area, fragmentation increases the edge to area comprising 4.5% of the land area. By contrast, in the ratio of surviving patches, leading to a smaller county of Dorset, pasture accounted for 28% of the effective undisturbed interior. Edge habitats may land area (716 km2, Fig. 1.3), meadows 1% (28 km2), be structurally and physically different from the and woodland 13% (328 km2). However, since interior with compacted or altered soil (including this anthropogenic expansion of grassland across agricultural run-off adjacent to crop fields), and a the English landscape, in the last 200 years there high density of woody vegetation. Fragmentation has been an even more dramatic decline in these can alter the natural disturbance regime; roads, now-valued semi-grasslands concomitant with the for example, provide a barrier to the spread of expansion of grassland ‘improvement’, conversion landscape fire. These environmental differences to cropland, and urbanization. For example, Fuller can lead to several direct and indirect effects on (1987) estimated that semi-natural pastures in the the flora and fauna including a high diversity of English lowlands declined by over 97% between exotic species, low diversity of native species, low 1930 and 1984. Although many of these areas still nest success, and high predation rates on native remained in grassland they had been improved birds. Fragmented populations may be genet- by seeding or management for agriculturally pre- ically isolated, reduced in size, and susceptible to ferred species, notably Lolium perenne and Trifolium inbreeding, genetic drift, and extinction. Reviews repens. Of the surviving semi-natural lowland INTRODUCTION 9
problem of invasion of grasslands by non-native species. In some cases, as noted above for the California prairie, exotics can completely replace the native species causing a fundamental alteration to the physiognomy and structure of the whole eco- system. In other cases, a single species may be more insidious, seemingly moving into vacant microhab- itats. Nevertheless, any exotic species introduction affects the complex dynamics of grassland to some extent (see § 9.2.4). The extent to which grassland is subject to invasion by exotic species depends in part on the severity of any changes in the envi- ronment or to the natural disturbance regime. Overgrazing, drought, infrequent fire, excessive Chalk downland region trampling, or other stresses can all allow exot- ics to establish; after which, changes can become Heathland region self-reinforcing (Chaneton et al. 2002; Weaver et al. 1996). Fragmentation, mentioned above, and Figure 1.3 Area of pasture in Dorset, England in 1086 as increased adjacency of other ecosystems such as recorded by the Domesday Book. Each black circle represents, agricultural land and forest, increases the influx at the scale of the map, the total area of pasture within each 10−km square. With permission from Rackham (1986). of exotics through dispersal. Although many exot- ics are introduced and spread accidentally, others are deliberately introduced. For example, seeding grasslands, communities of special floristic interest with exotic species is used to rehabilitate degraded represented only 1–2% (Blackstock et al. 1999). pastures in Australia (Noble et al. 1984). Medicago Other areas around the world where species- spp. have been widely used in winter rainfall, semi- poor grassland of low conservation value has arid zones with success, but the species have subse- expanded include the pastures of the eastern and quently become widely naturalized. 6 south-eastern USA in which over 14 10 ha of The total extent to which exotic species have the introduced European Schedonorus phoenix (syn. altered grasslands is unclear except where whole- Festuca arundinacea) has been planted (Buckner and sale changes are evident as with the California 6 Bush 1979). Similarly, in California, 10 10 ha of prairie noted earlier. Floristically, the magnitude native California prairie once characterized by of exotic species invasion in grassland can be high. perennial bunchgrasses including Nassella pulchra For example, 17% (70 of 410) of plant species on the and N. cernua is now dominated by exotic annual Pawnee National Grasslands in eastern Colorado, grasses, including Avena fatua, A. barbata, Bromus USA, and 28% (16 of 56) of grasses in Badlands mollis, B. diandrus, B. rubens, Hordeum marinum, National Park, South Dakota, USA are exotics H. murinum, H. pusillum, and Vulpia myuros (Heady (Licht 1997). Of 100 organisms listed as the ‘world’s 2 et al. 1992). Sown pastures cover 436 000 km (5.6%) worst’ exotics, 13 land plants that invade grassland in Australia, none of which were present before were included (Table 1.8). the arrival of European settlers in 1780 (Gillison In addition to the widespread exotics listed in 1992). In temperate areas, these sown pastures are Table 1.8, numerous other exotics have invaded, dominated by European species including Lolium become naturalized, and altered native grasslands perenne and Trifolium repens. To the range manager on a more regional basis; these include the follow- these planted exotics are beneficial as they can pro- ing (Poaceae except where indicated): vide nutritious forage year round. However, to many conservationists, the exotic ● Centaurea spp. (knapweeds: Asteraceae) and species listed above are indicative of the larger other thistles including Cirsium vulgare and Carduus Table 1.8 ‘World’s worst’ invasive land plants of grassland
Name Common name Family Life form Origin Where it’s invading
Arundo donax (L.) Giant cane Poaceae Perennial grass Indian subcontinent Subtropical and temperate principally in riparian zones and wetlands, but also chaparral, oak savannahs, and pastures in South Africa and the United States. Chromolaena odorata (L.) Agonoi Asteraceae Perennial shrub Central and South Pastures in tropical Africa and Asia King and Robinson America Fallopia japonica var. Donkey rhubarb Polygonaceae Herbaceous Japan Dense clumps in riparian areas, woodland, and grassland japonica (Houtt.) Ronse perennial in most of North America, Northern Europe, Australia and Decraene New Zealand. Spreads along river banks, and into derelict/ development land, amenity areas and roadsides. Hedychium gardnerianum Kahila garland-lily Zingiberaceae Herbaceous Eastern Himalayas Wet habitats in the Federated States of Micronesia (Pohnpei), Ker (Himal.) perennial French Polynesia and Hawaii, New Zealand, South Africa, La Réunion, Jamaica and the Azores islands. Recorded from improved pastures in New Zealand. Imperata cylindrica (L.) Beauv. Alang-alang Poaceae Perennial grass SE Asia, Philippines, Throughout the temperate and tropic zones (particularly the China and Japan SE US) in all habitats from dry flatwoods to the margins of permanent bodies of water. Alters the natural fire regime, producing intense heat when it burns. Lantana camara L. Largeleaf lantana Verbenaceae Ornamental shrub SW USA, Central and Weed of pastures and other habitats in >50 countries South America throughout tropics, subtropics and temperate regions. Decreased productivity of pastures and poisons cattle. Leucaena leucocephela (Lam.) Leucaena Fabaceae Tree Mexico and Central Widely promoted for tropical forage and reforestation, now De Wit America spreading widely in >20 countries across all continents except Europe and Antarctica. Problem in open (often coastal or riverine) habitats, semi-natural, disturbed, degraded habitats and other ruderal sites. Specifically noted invading grasslands in Ghana, Florida, and Hawaii ha in eastern USA, $500 million million $500 USA, eastern in ha 6 d, now invading shrubland, forests, and grassland forests, grassland shrubland, and invading now d, and pastures in Australia, India, Bangladesh, Sri Lanka, Mauritius, Thailand, the Philippines, Malaysia, Indonesia, Papua New Guinea, and many of the Pacific islands well as undisturbed natural vegetation including pastures and grassland Asia. Invades and spreads along watercourses and seasonally the In regions. subtropical and tropic in wetlands flooded Northern Territories of Australia it is a problem in grassland (Mitchell grass) and low Eucalyptus and Melaleuca savannah Norfolk Island, and peninsular Florida. A problem mostly in forests, but also invades grassland in south Florida and Micronesia in South Africa, Chile, Australia, New Zealand. Regenerates profusely after fire and severely depletes the local water table estimated losses per Also year. in Japan and New Zealand. Invades all habitats, including pastures, except periodically areas flooded A weed of tea, rubber, oil palm and other crops, and forests Southern USA, Hawaii, and Spain. Pioneer of disturbed sites as Introduced to Australia, and many countries in Africa and Widespread across 2–3 10 2–3 across Widespread S. AmericaS. Brazil South America Mediterranean Widely plante Brazil Mauritius, Hawaii, Polynesia, the Mascarenes, Seychelles, small treesmall Mile-a-minute weed Asteraceae Perennial vine Central and Brazilian hollyBrazilian Anacardiaceae Tree Argentina, Paraguay, Catclaw mimosa Fabaceae Woody shrub Mexico, Central and Kudzu Fabaceae vine Semi-woody Asia Sabine Strawberry guava Myrtaceae Evergreen shrub or (L.) (L.) Aiton. pine Cluster Pinaceae Tree L. (Willd.) Maesen & S. Kunth. Raddi lobata lobata Almeida
Mikania micrantha Mikania pigra Mimosa Pinus pinaster Psidium cattleianum var. montana Pueraria Schinus terebinthifolius (2003). Group Specialist Species Invasive IUCN/SSC From 12 GRASSES AND GRASSLAND ECOLOGY
● acanthoides—rangeland of the US Midwest and regulating services (e.g. sequestration of CO2, pre- rolling Pampas of Uruguay (Lejeune and Seastedt vention of soil loss, maintenance of soil fertility) 2001; Soriano 1992). ● provisioning services (e.g. plant materials and ● Annual grasses including Bromus spp. (brome, game) cheat grass), Avena fatua (wild oat)—throughout ● cultural services (e.g. ecotourism, scenery, reli- North American and Canadian grasslands, espe- gious value). cially in the west (Hulbert 1955; Mark 1981). A problem is that many of the most valuable ● Annual legumes (Fabaceae) Medicago spp. (medic), services are precisely those that have no clear mar- Stylosanthes spp. (pencilflower), and Trifolium spp. ket value (Sala and Paruelo 1997). On the basis of (clover), and perennials including Lolium perenne 17 ecosystem services and functions, the estimated (perennial ryegrass), Dactylis glomerata (cocksfoot), the total value of the grass/rangeland biome was and Trifolium repens (Fabaceae, white clover)— $232 ha–1 yr–1 (1997 $s); considerably less than forests naturalized following introduction in modified ($969 ha–1 yr–1) and wetlands ($14 785 ha–1 yr–1), but native grasslands and pastures in temperate and 2.5 times that of cropland ($92 ha–1 yr–1) (Costanza tropical Australia (Donald 1970; Moore 1993). et al. 1997). Other, less controversial, economic ● Acaena magellanica (bidibid, Rosaceae, New models which specifically incorporate the value Zealand native)—forms dense carpets replacing of grasslands include those of Ogelthorpe and once extensive Poa cookii and Pringlea antiscorbutica Sanderson (1999), and Herendeen and Wildermuth communities in sub-Antarctic islands (Hnatiuk (2002). Of these, Ogelthorpe and Sanderson’s (1999) 1993). study is unique in combining a ecological-based ● Sporobolus indicus (wire grass, South African floristic model based on the composition of grass- native)—with the exotic woody Psidium guayava land vegetation types with a more conventional Raddi (Myrtaceae) dominates hills on Viti Levu management model to cost the supply of desired and other Fijian islands (Gillison 1993). goods (ewes and lambs for market) and derive ● Acacia mearnsii (black wattle, Australian native)— optimum policy. By contrast, Herendeen and cost of watershed invasion in South Africa esti- Wildermuth (2002) conducted an economic analysis mated at $1.4 billion in water lost to impoundments of an agricultural county in Kansas, USA, develop- through transpiration (de Wit et al. 2001). ing energy, water, soil, and nitrogen budgets. They showed that grazed rangeland (70% of county land 1.4 Grassland goods and services area) was essentially self-sustaining, contributing little to any depletion of resources, independent All grasslands are dominated by members of the of outside subsidies, and not disruptive of natural Poaceae family, the fifth most speciose family cycles. This contrasted sharply with other activities ( 7500 species) (Chapter 2), and the most wide- including row crop agriculture. spread. Grasses are also the most important food Williams and Diebel (1996) considered the eco- crop on earth, with corn, wheat, maize, rice, and nomic value of grassland under two categories: use millet accounting for most crops grown for food. value and non-use value. The former includes serv- (The Fabaceae with the legumes including soybean, ices that people obtain from direct interaction with beans, lentils, pulses, and peas are also important the grassland resource and consist of grazing live- food crops and perhaps come second.) stock, harvesting native or cultivated plants, hunt- Efforts at assigning an economic value to ecosys- ing wildlife, recreational activities (e.g. hiking, bird tems and ecosystem functions (Costanza et al. 1997) watching, photography), educational activities, ero- are difficult and uncertain at best, and certainly sion control and water quality enhancement, and controversial (Pimm 1997; Sagoff 1997). Ecosystem research activities. By contrast, non-use values are services and functions can be categorized into four those associated with intangible uses and include: groups (Farber et al. 2006): existence and option, aesthetics, cultural-historical ● supportive functions and structures (e.g. nutrient and sociological significance, ecological or biologi- cycling, primary production, pollinator services) cal mechanisms, and biological diversity (see § 7.1.3 INTRODUCTION 13 and § 9.1). The authors bemoaned the difficulty of densities in the world in the Middle East, Asia, pricing these services but concluded that account- and Australia (White et al. 2000). Recent trends ing for these resources in economic indices would (1986–1988) include an average 5.6% increase in be critical for prairie conservation. The debate on livestock numbers in developing countries with pricing ecosystem functions, goods, and services extensive grassland. Some of the largest increases continues to consider the efficacy of integrating include Mongolia, where cattle increased by 40% economic and ecological components (Costanza and sheep and goats by 31.5% over this period. The and Farber 2002; Farber et al. 2006, and papers largest increase was seen in Guinea where live- therein). stock increased by 104%. Although these increases In a more general sense, occupying such a large may reflect somewhat improved economic condi- area of the earth’s surface, grassland ecosystems tions in these countries, they are also indicative provide many important goods and services that of overgrazing and a degraded range. White et al. can be quantified, at least to some extent. These (2000) estimate that 49% of grasslands worldwide are considered below under four broad headings were lightly to moderately degraded, with at least (White et al. 2000): food, forage and livestock, 5% strongly to extremely degraded. biodiversity, carbon storage, and tourism and As a source of forage for livestock, whether grazed recreation. Other important functions of grass- directly or harvested for consumption elsewhere lands include the provision of drinking and irri- (e.g. feed lots), there is a long-standing apprecia- gation water, genetic resources, amelioration of tion and dependence in agriculture for grasslands the weather, maintenance of watershed functions, (Flint 1859). In the USA, forage accounts for about nutrient cycling, human and wildlife habitat, 57% of the total feed of beef cattle (Barnes and removal of air pollutants and emission of oxygen, Nelson 2003). Dairy cattle use a somewhat lower employment, soil generation, and a contribution proportion of forage in their diet (c.16%) than do to aesthetic beauty (Sala and Paruelo 1997; World beef cattle, swine (13%), poultry ( 5%), horses and Resources 2000–2001). mules (3%), and sheep and goats (2%). The value of forages in the USA is $27.8 billion (1998 estimate), and exceeds the value for other crops. Hay accounts 1.4.1 Food, forage, livestock, and biofuels for $11.7 billion, exceeded only by the value of corn The most widespread use of grassland worldwide is and soybeans in the market ($19.1 and $14.7 billion, in the production of domestic livestock (principally respectively) (Barnes and Nelson 2003). mammalian herbivores: cattle, sheep, goats, horses, There is a large variety of forage plants, and for water buffalo, and camels). In addition, large num- the most part they are grasses or legumes (Moore bers of wild herbivores also depend on grasslands, 2003). In Europe, Australia, and New Zealand, the and in many cases share the land with domestic most important forages are Lolium perenne (peren- herds. Wild native herbivores are regarded as nial ryegrass) and Trifolium repens (clover). In the beneficial, adaptive, or even critical for grasslands. north-eastern USA introduced cool-season spe- For example, the American bison is considered a cies, particularly white clover and Kentucky blue- keystone species for the US tallgrass prairie (see grass Poa pratensis are important, with introduced § 9.3.1). The non-economic benefit to grasslands warm-season species including Cynodon dactylon (e.g. enhanced biodiversity) of introduced domes- (Bermuda grass), Paspalum dilatatum (dallisgrass), tic livestock is less clear (McIntyre et al. 2003), Paspalum notatum (bahiagrass), and Sorghum and in the common case of overgrazing, is clearly halepense (Johnsongrass) becoming predominant in detrimental. Certainly, however, in subsistence the south-eastern USA (Barnes and Nelson 2003). rangeland economies, domestic livestock serve The cool-season Schedonorus phoenix (tall fescue) many benefits in addition to food and cash includ- is the most widely planted forage in the transi- ing dung for fuel and flooring (Milton et al. 2003). tion between the north-eastern and south-eastern The densities of livestock in grasslands range regions, whereas in the mid-west and western from 1 to 100 head/km2, with the highest USA several native warm-season prairie grasses 14 GRASSES AND GRASSLAND ECOLOGY remain dominant such as Andropogon gerardii (big photosynthesis (Chapter 4), high water-use effi- bluestem) and Sorghastrum nutans (Indian grass), ciency, partitioning of nutrients below ground in which are replaced towards the west with shorter the dormant season, lack of known pests or dis- grasses such as Bouteloua gracilis (blue grama) and eases, rapid spring growth, long canopy duration, Bouteloua dactyloides (syn. Buchloe dactyloides, buf- sterility, and perennial life form. The forage from falograss) in the south and Agropyron spp. and these bioenergy crops allows the production of Pseudoroegneria spp. (wheatgrasses), and Elymus clean-burning liquid biofuels including ethanol spp. (wildryes) in the north. A wide variety of for generating heat and electricity and as a trans- native and introduced species are used as forage portation fuel. The energy content of biofuels is in tropical regions and these include Chloris gayana 17–21 MJ kg–1, which compares favourably with (Rhodes grass), Cynodon dactylon, Digiitaria decum- the energy content of fossil fuels (21–28 MJ kg–1). bens (Pangola grass), Panicum maximum (Guinea It has been estimated that if only 20% of the cur- grass, zaina), and Pennisetum clandestinum (Kiyuku rent agricultural land in the state of Illinois were grass) (Skerman and Riveros 1990). A wide variety planted to Miscanthus, 145 TWh of electricity could of legumes are planted as forage, with over 30 gen- be generated which exceeds the 137 TWh of elec- era often planted in mixture with grasses in the tricity consumed annually by the state including tropics alone (Skerman et al. 1988). Because of their Chicago, the third largest US city (Heaton et al. association with Rhizobium spp. bacteria, legumes 2004). The potential economic and environmental are highly nutritious and can increase levels of benefits of using bioenergy crops include near- nitrogen in the soil (Skerman et al. 1988). Important zero emissions of greenhouse gases (the carbon species include Trifolium repens and T. pratense emitted from burning the crop biomass is equal (white and red clover), Medicago sativa (alfalfa), to or less than the carbon fixed via photosynthe- Lespedeza spp. (annual and perennial lespedezas), sis to produce the biomass), and improved carbon Vicia sativa (common vetch), Lotus corniculatus sequestration and soil and water quality. Economic (birdsfoot trefoil) in temperate areas (Moore 2003; estimates for using P. virgatum in the USA predict Rumbaugh 1990), and Centrosema pubescens (Centro, an annual increase in net farm returns of $6 bil- butterfly pea), Pueraria phaseoloides (trop ical kudzu), lion, a decrease in government farm subsidies of Stylosanthes guianensis (Schofield stylo, Brazlian $1.86 billion, and a reduction of 44–159 Tg yr–1 of stylo), and S. hamata (Caribbean stylo) in the tropics greenhouse gas emissions (McLaughlin et al. 2002). (Skerman et al. 1988; Skerman and Riveros 1990). Of Bioenergy crops do not require replanting for 15 these forage legumes, M. sativa is the most wide- years and can be harvested annually for biomass. spread as it is planted on 32 106 ha worldwide, As in native prairie (Chapter 7), planting these with the most widespread plantings in the USA perennial grasses leads to large amounts of below- (13.3 106 ha) (Michaud et al. 1988). ground carbon sequestration with higher levels of A number of perennial grasses are used increas- organic carbon and nitrogen in the soil than con- ingly in Europe and North America as renewable ventional crops like corn (see § 1.4.3). The seques- bioenergy sources, as they can be grown with tered soil carbon has potential use as a carbon minimal maintenance on marginal soils and har- credit. Emissions of CO2 from burning bioenergy vested to produce large volumes of carbon-rich bio- crops are substantially lower than from conven- mass. These bioenergy crops include a number of tional sources; for example, CO2 emissions from high biomass, rhizomatous bunchgrasses such as P. virgatum were estimated at 1.9 kg C GJ–1 com- miscanthus Miscanthus spp., switchgrass Panicum pared with 13.8, 22.3, and 24.6 1.9 kg C GJ–1 from virgatum, kleingrass P. coloratum, buffalograss gas, petroleum, and coal, respectively (Lemus and Bouteloua dactyloides, elephant grass Pennisetum Lal 2005). Although planting grasses as biofuels has purpureum, reed canarygrass Phalaris arundinacea, economic and environmental advantages, the eco- big bluestem Andropogon geradii, giant reed Arundo logical traits of a biofuel species (described above) donax, and tall fescue Schedonornus phoenix. Ideal are also known to contribute to invasiveness, bioenergy crops share the ecological traits of C4 prompting concerns regarding the ecological risks INTRODUCTION 15
involved in introducing and planting them (Raghu ● Perhaps the biologically richest grassland world- et al. 2006). Many of the biofuel species listed above wide is that of the Agulhas Plain, part of the Cape are invasive outside their native range. Floristic Province of South Africa. This region, Native grassland has the potential to be a considered as one of the world’s 25 biodiversity valuable bioenergy source. Mixtures of native grass- hotspots for conservation (Myers and Mittermeier land perennials, referred to as low-input high- 2000), contains a flora of 1751 species, including diversity (LIHD) biofuels, were shown to exhibit 23.6% regional endemics and 5.7% local endem- bioenergy yields 238% greater than monocultures. ics (Cowling and Holmes 1992) in a landscape of Moreover, these LIHDs are carbon negative with shrubland, savannah, and fynbos (Rouget 2003).
● more CO2 sequestered in the soil and roots (4.4 Mg By contrast, some grasslands, such as those of –1 –1 CO2 ha yr ) than released during conventional the US Great Plains, are of relatively recent origin –1 –1 biofuel production (0.32 Mg CO2 ha yr ) (Tilman and so support comparatively few species and low et al. 2006a). levels of endemism (Axelrod 1985). Nevertheless, species in the Great Plains tend to be character- ized by high levels of ecotypic differentiation (e.g. 1.4.2 Biodiversity Gustafson et al. 1999; Keeler 1990, McMillan 1959b, By any measure, the world’s grasslands qualify as and see Chapter 5; ) adding to the biological rich- important repositories of biodiversity. As noted ness and the value of the system (Risser 1988). earlier and discussed in more detail in Chapter 2, As with other biomes, there is growing con- the major cereal crops of the world are grasses, cern over the loss of biodiversity through habitat and their ancestors arose in grasslands. Modern loss and alteration (see above). White et al. (2000) improvement of cereal and forage cultivars through identified 697 areas worldwide that were at least breeding continues today to draw upon the genetic 10 km2 in size and 50% grassland cover that were reserves in grasslands. afforded IUCN category I, II, or III level of protec- The richness of grassland biodiversity is exem- tion (i.e. nature reserve, wilderness area, national plified by the following observations summarized park or monument status). These areas totalled from White et al.’s (2000) analysis: 3.9 106 km2, more than the 1.6 106 km2 of simi- ● Forty of the world’s 234 Centres of Plant Diversity larly protected forest, but only 7.6% of the total (CPD) identified by the International Union for 52 106 km2 of grasslands worldwide. The largest Conservation of Nature and Natural Resources area of protected grasslands is 1.3 106 km2 in sub- (IUCN)-World Conservation Union and World Saharan Africa. On a percentage basis, the high- Wildlife Fund-US occur in grasslands, with an addi- est level of protection is in North America where tional 70 CPDs containing some grassland habitat. 0.8 106 km2 of 6.6 106 km2 (12%) is protected. To qualify as a CPD mainland areas must contain Nevertheless, within the Great Plains there are 1000 vascular plants with 10% endemism. large differences in the level of protection afforded ● Grassland/savannah/scrub is the main habitat in different grasslands; in 1994 only 0.07% (91.8 km2) 23 of 217 Endemic Bird Areas identified by Birdlife of Tamaulipus Texas semi-arid plain was protected International, of which 3 have the highest rank for (at any level), compared with 13.3% (120 000 km2) biological importance (Peruvian High Andes, cen- of west- central semi-arid prairies (Gaulthier and tral Chile, and southern Patagonia). Wiken 1998). Of the different grasslands worldwide, ● Thirty-five of 136 terrestrial ecoregions identi- temperate grasslands are afforded the least protec- fied on the basis of outstanding diversity and as tion (0.69%), ranging from 0.08% in the Argentine priorities for conservation by the World Wildlife Pampas to 2.2% in the South African grassveld Fund-US Global 200 programme are grassland. (Henwood 1998b). Not surprisingly, there is grow- ● Ten of 32 North American and 9 of 34 Latin ing concern at this poor level of protection with the American grassland ecoregions are rated as glo- IUCN and World Commission on Protected Areas bally outstanding for biological distinctiveness by taking a lead role in raising public awareness of the World Wildlife Fund-US. the problem and organizing the political will 16 GRASSES AND GRASSLAND ECOLOGY to protect more grassland (e.g. Henwood 1998a; of years (see § 7.3). Above ground, low-latitude IUCN-WCPA 2000) areas have high production because of the higher temperatures, but below-ground storage is low. The total global carbon store in grasslands is 1.4.3 Carbon storage comparable to that in forests because grassland A global service of grasslands and other ecosys- areas are so extensive worldwide, but on a unit tems is the storage of carbon. Through photosyn- area basis it is less, although still comparable to thetic fixation of CO2, producers remove carbon that of agroecosystems. Thus, grasslands are a from the atmosphere. Simultaneously, respiration potentially important sink for carbon in the ter- recycles carbon, again as CO2, back into the atmos- restrial biosphere, a fact of particular importance phere. As the basis for life, the efficient operation given the increase in anthropogenic increase in of the global carbon cycle is critical. Its successful atmospheric carbon since the beginning of the operation depends also on three carbon reservoirs, Industrial Revolution (IPCC 2007). The extent and namely the atmosphere, the oceans, and the ter- time frame over which terrestrial carbon sinks, restrial biosphere. This overly simplistic descrip- including grasslands, will change in response to tion of the carbon cycle (more details can be found global climate change is uncertain, but a mat- in most general ecology textbooks, and see § 7.2) ter of concern (Grace et al. 2001a). Uncertainty should, however, be sufficient to emphasize the lies in predicting changes in decomposition and importance of this cycle. photosynthetic rates to changing CO2, tempera- Grasslands provide a significant service towards ture, and nutrient supplies (e.g. altered nitrogen global carbon storage by virtue of high levels of availability). carbon accrual and sequestration below ground The high organic matter content of grassland in the soil. Up to 90% of grassland biomass is soils has been their Achilles heel in some respects, below ground (see § 7.1.2), and levels of soil car- as it led to widespread cultivation in areas such as bon are higher in grasslands than in forests, the North American Great Plains. Conventional agroecosystems, or other ecosystems (Table 1.9). tillage practices oxidize soil organic matter, and, as Carbon storage below ground is particularly a result, soil carbon has declined 20–60% in former high at high latitudes where decomposition rates grasslands that have been cultivated (Burke et al. are generally low and soil organic matter and 1995; Mann 1986). Recovery to steady-state condi- hence carbon stocks can build up over thousands tions of the active soil carbon pool after cultivation
Table 1.9 Carbon storage of grasslands compared with forests and agroecosytems. Values are in Gt C and show minimum and maximum estimates
Ecosystem Vegetation Soils Total C stored/area (t C/ha)
Grasslands High-latitude 14–48 281 295–329 271–303 Mid-latitude 17–56 140 158–197 79–98 Low-latitude 40–126 158 197–284 91–131 Total 71–231 579 650–810 123–154 Forests 132–457 481 613–938 211–324 Agroecosystems 49–142 264 313–405 122–159 Othera 16–72 160 177–232 46–60 Global total 268–901 1484 1752–2385 120–164
a Includes wetlands, barren areas, and human settlements. Adapted from White et al. (2000). INTRODUCTION 17 can take 50 years or more after restoration with countries with grasslands making up 80% or more native perennial grasses under the US Conservation of the land area, the numbers of international tour- Reserve Program (Baer et al. 2002). In this study, the ists between 1995 and 1997 ranged from 10 000 per labile carbon pool resembled native prairie within year in Somalia to 4.0 106 in Australia (Table 1.5). 12 years of restoration. Other causes of carbon loss Over the 10-year period from 1985–1987 to 1995–1997 from grasslands include fire, grazing, and exotic the numbers of international tourists entering these species. Burning savannahs, for example, releases countries increased by 150% (Benin) to 331% (Central carbon to the atmosphere, and contributes up to African Republic). Somalia was an exception, with
42% of gross CO2 to global emissions (White et al. tourist numbers decreasing 74%, hardly surprising 2000). Sala and Paruelo (1997) estimated carbon given the political problems in the country (civil sequestration in grasslands of eastern Colorado, strife and famine). Similarly, where figures are USA to be worth c.$200 ha–1, quite a bit more than available for these countries, international tourism the average cash return of $47 ha–1 yr–1 from meat, receipts ranged from US$5 106 to US$8503 106 wool, and milk. The loss of carbon from grassland per year during 1995–1997 in the Central African soils to the atmosphere occurs rapidly following Republic and Australia, respectively, reflecting conversion to cropland, but the reverse process of a change from 1985–1987 of –7% (Benin) to 471% carbon accrual following agricultural abandon- (Australia) (data for Somalia were unavailable) ment is very slow (60 kg C ha–2 yr–1), with the sys- (Table 1.5). In addition to visits and money spent, the tem regaining its original value at a rate of only numbers of safari hunters and revenues from the $1.20 ha–1 yr–1. Grasslands take up more methane hunting industry also increased over this period. and emit less nitrous oxide than cropland at an Although these data do not prove a positive rela- estimated cost of $0.05 ha–1 yr–1 and $0.60 ha–1 yr–1 tionship between the occurrence of grassland and respectively (Sala and Paruelo 1997). tourism or recreation, they are certainly consistent with the idea that grasslands provide this service. The general consensus from conservation agencies 1.4.4 Tourism and recreation such as the World Resources Institute is that tour- Increasingly, grasslands provide a destination for ism and recreation represent a significant economic tourists (ecotourism) and a location for recreational grassland service, but that the continued decrease activities including hiking, fishing, viewing of in grassland extent and biodiversity raises serious game animals, safaris, cultural and spiritual needs, concern about a potential decline in the capacity of and aesthetic enjoyment. Ecotourism is defined as grasslands to maintain these services over the long ‘responsible travel to natural areas that conserves term (World Resources 2000–2001). the environment and improves the well-being of The attractiveness of grasslands and the willing- the local people’ (Honey 1999). It is characterized ness of tourists to pay to view large herbivores such by its benefits to the visitor as well as conservation as elephants provide a powerful incentive for land- and the people of the host country. Honey (1999) owners to develop environmental business oppor- identifies seven characteristics of ecotourism: (1) tunities. For example, game farms adjacent to South involves travel to natural destinations, (2) minim- Africa’s Kruger National Park generate 15 times the izes impact, (3) builds environmental awareness, income from tourism and employ 25 times more (4) provides direct financial benefits for conserva- people than cattle farming (Milton et al. 2003). In tion, (5) provides financial benefits and empow- some countries with large expanses of grassland erment for local people, (6) respects local culture, habitat, such as Namibia in which 13% of the coun- and (7) supports human rights and democratic try is set aside for nature conservation, tourism is movements. one of the most important sectors of the economy The importance of grasslands in meeting these (Barnes et al. 1999). The Etosha National Park, an criteria is difficult to gauge accurately, but some of area of desert grassland in Namibia, was the most the useful indicators include the number of tourists important specific attraction named by visitors and the money that they spend. In an assessment of surveyed, following their preference for unique, 18 GRASSES AND GRASSLAND ECOLOGY unspoiled nature/landscape and wildlife/animals destination since the 1960s (point 1). However, (Barnes et al. 1999). Similarly, in Botswana where recent civil unrest (2007–8) has seriously damaged Kalahari savannah and woodland dominate the the tourist industry, and protected areas have suf- landscape, wildlife viewing was estimated to have fered from over-exploitation, poaching, and poor a clear economic advantage over cattle farming management (point 2), resulting in little concern on about one-third of wildlife land (Barnes 2001). for the needs and human rights of the rural farm- Ecotourism is an economically significant and fast- ers and pastoralist (points 6 and 7) or environmen- growing component of the economy, especially in tal protection (point 4). On the positive side, Kenya rural areas, of an increasing number of developing has conducted a number of innovative ecotour- countries with extensive areas of grassland (Kepe ism experiments such as community conservation 2001). In developed countries, too, the economic schemes that have had some success (point 5) and merit of ecotourism in habitats containing grass- raised environmental awareness at least among land is increasingly considered a viable and appro- some segments of the population (point 3). priate land use (Norton and Miller 2000). Wildlife tourism to the Serengeti grassland 1.5 Early grassland ecologists in central Africa is providing an economic boost to Tanzania, one of the poorest countries in the Many early ecologists and botanists were inter- world. The Serengeti National Park, with an area ested in grassland. We can go back to Charles of 14 763 km2 contains some 4 106 animals, Darwin’s comments lamenting the invasion of including migratory zebras Equus burchelli, elands exotic thistles in the Pampas of Argentina (Darwin Taurotragus oryx, and wildebeest Connocheatas 1845). However, two early grassland ecologists taurinus along with free-roaming lions Panthera come to mind as having significantly influenced leo, elephants Loxodonta africana and other graz- the subsequent development of the discipline. This ing ungulates such as Thomson’s gazelle Gazella section will briefly outline the life and times, and thompsonii and buffalo Syncherus caffer, spread contributions, of J.E. Weaver (North America) and across a tropical/subtropical bunchgrass savan- J.W. Bews (South Africa). Coincidentally, both men nah dominated by grasses including Themeda tri- were born in the same year, 1884; the year that anda (McNaughton 1985) (see § 6.1 and Plate 4). The Mark Twain’s Huckleberry Finn was published, that Serengeti is one of 12 national parks and 14 game Belize became a British colony (until 1981), that the reserves in Tanzania, all of which are at the heart of Statue of Liberty was unveiled in New York, and a tourism boom. Honey (1999) assessed the success the 17-year old pianist and composer Scott Joplin of Tanzania in meeting the 7-point criteria for eco- arrived in St Louis. tourism concluding that the country ranked high on points 1 and 3 (involves travel and builds envir- 1.5.1 John William Bews onmental awareness) and was making reasonable progress towards attaining points 2, 4, 5, and 7 J.W. Bews (1884–1938), MA, DSc, Professor of Botany (minimal impact, financial benefit for conservation in the Natal University College, Pietermaritzburg, and local people, and support of human rights), but South Africa, was a pioneer in plant ecology in was doing poorly with regard to point 6 (respect South Africa. He was originally from the Orkney of local culture). Specifically, the local Masai peo- Islands off the north coast of Scotland, and had ple, despite being at the forefront of ecosystem academic training at the University of Edinburgh. preservation, remain the subject of prejudice and Bews published widely on the floristics, ecol- are viewed more as a tourist attraction than as a ogy, and systematics of South African vegetation valued and important cultural group in their own (Table 1.10) (Gale 1955). His highly original ideas right. By contrast, in neighbouring Kenya, which on human ecology were influenced by the general, owns the northern part of the Serengeti, the ecot- politician, and botanist Jan Christian Smuts (Anker ourism scorecard report is somewhat worse. Kenya 2000). His contributions were recognized by the has been Africa’s most popular wildlife tourism award of the South Africa Medal (Gold) in 1932. INTRODUCTION 19
Table 1.10 Selected books and monographs by John W. Bews and John E. Weaver (as single author except where indicated)
John W. Bews 1913 An oecological survey of the midlands of Natal, with special reference to the Pietermaritzburg district. Annals of the Natal Museum 2, 485–545 1916 An account of the chief types of vegetation in South Africa, with notes on the plant succession. Journal of Ecology 4, 129–159. 1917 The plant ecology of the Drakensberg range. Annals of the Natal Museum 3, 511–565. 1918 The grasses and grasslands of South Africa. P. David & Sons, Printers, Pietermaritzburg 1920 The plant ecology of the coast belt of Natal. Annals of the Natal Museum 4, 367–469. 1921 An introduction to the flora of Natal and Zululand. City Printing Works, Pietermaritzburg 1923 (with R.D. Aitken) Researches on the vegetation of Natal. Series I. No. 5. Government Printing and Stationery Office, Pretoria 1925 (with R.D. Aitken) Researches on the vegetation of Natal. Series II. No. 8. Government Printing and Stationery Office, Pretoria 1925 Plant forms and their evolution in South Africa. Longmans, Green, London 1927 Studies in the ecological evolution of the angiosperms. Wheldon & Wesley, London 1929 The world’s grasses; their differentiation, distribution, economics and ecology. Longmans, Green, London 1935 Human ecology. Oxford University Press, London 1937 Life as a whole. Longmans, Green, London John E. Weaver 1918 (with R.J. Pool and F.C Jean) Further studies in the ecotone between prairie and woodland. University of Nebraska, Lincoln, NE 1929 (with W.J. Himmel) Relation between the development of root system and shoot under long- and short-day illumination. American Society of Plant Physiologists, Rockville, MD 1930 (with W.J. Himmel) Relation of increased water content and decreased aeration to root development in hydrophytes. American Society of Plant Physiologists, Rockville, MD 1932 (with T.J. Fitzpatrick) Ecology and relative importance of the dominants of tallgrass prairie. s.n., Hanover, IN 1934 (with T.J. Fitzpatrick) The prairie. Prairie/Plains Resource Institute, Aurora, NE (reprinted 1980) 1938 (with F.E. Clements) Plant ecology. McGraw-Hill, New York 1954 North American prairie. Johnsen Publishing, Lincoln, NE 1956 (with F.W. Albertson) Grasslands of the Great Plains: their nature and use. Johnsen Publishing, Lincoln, NE 1968 Prairie plants and their environment; a fifty-year study in the Midwest. University of Nebraska Press, Lincoln, NE
This prestigious award recognizes the exceptional was then known about the floristics and ecology contribution to the advancement of science, on a of grasslands in South Africa (Bews 1918), but in a broad front or in a specialized field, by an eminent longer treatise produced a general worldwide clas- South African scientist. He was the first principal sification of grassland vegetation (Bews 1929). His of the University of Natal, where his legacy lives on ‘phylogenetic arrangement’ of world grasslands in the John Bews Building that houses the faculties was derived from Schimper’s early classification of science and agriculture and their library. which divided the vegetation of the world into Bews conducted extensive floristic work, some woodland, grassland, and desert. Bews incorpo- of the first on the grassland plant communities of rated the then current understanding of grass evo- South Africa. A strong proponent of Clementsian lution with Clementsian ideas on the successional succession, the second stage of Bews’s grassland relationships between forests and grasslands. As work dealt with the developmental history of the a result he produced a vegetation classification various plant communities. His grassland work is which allows accommodation of grasslands from important because he not only summarized what around the world. The classification was essentially 20 GRASSES AND GRASSLAND ECOLOGY a functional type approach that can be used today composition (Weaver 1954; Weaver and Albertson (see Chapter 8). He also placed the systematics of 1956). His drawings and photographs of excavated grasses into the context of angiosperm evolution in root systems have never been equalled, and are a series of papers (Bews 1927, collected together in superseded only perhaps through the use of more book form in the same year). modern techniques for tracking root system devel- opment (Chapter 3). He was particularly concerned with the effects of grazing (Weaver and Tomanek 1.5.2 John Earnest Weaver 1951) and the ‘great drought’ of 1934 (Weaver and J.E. Weaver (1884–1966), Professor of Plant Ecology Albertson 1936, see § 9.4). Much of his work was at the University of Nebraska, was a pioneer published as substantial, lengthy articles and mon- ecologist of the North American tallgrass prairie. ographs. Fondly remembered by over 100 master’s He studied the prairie for over 50 years, leaving and doctoral students, he is said to have remarked a legacy of 100 publications including 17 books of the prairie ‘look carefully and look often’ (Voigt (Table 1.10). His work covered every aspect of 1980). He was honoured as Research Associate with prairie ecology, and he is remembered today for the Carnegie Institute of Washington, President of his detailed study of plant root systems (Weaver the Nebraska Academy of Sciences, President of 1958, 1961; Weaver and Darland 1949a), competi- the Ecological Society of America, and honorary tion between plants (Weaver 1942), and community President of the International Botanical Congress. CHAPTER 2 Systematics and evolution
. . . the study of grass classification or taxonomy does Flagellariaceae (see §2.4.1) as well as the familiar more than satisfy our curiosity about the diversity of liv- Juncaceae, Cyperaceae, and Bromeliaceae (Stevens ing things and the way in which they have evolved. 2001 onwards). The systematic groups within the Stebbins (1956) family are still in a state of flux, but 7500 to 11 000 species are recognized depending on the authority, The rapid development as far as we can judge of all the divided among 600–700 genera within 25 (some- higher plants within recent geological times is an abom- times 50) tribes and 12 subfamilies (3–12) (Flora inable mystery. of China Editorial Committee 2006). The larg- Charles Darwin, letter to Sir Joseph Hooker (1879). est genera are Panicum (panic grass, c.500 spp.), Poa (bluegrass, c.500 spp.), Festuca (fescue, c.450 Grasses are the dominant plants of grasslands spp.), Eragrostis (lovegrass, c.350 spp.), Paspalum (Chapter 1) and of agriculture. The systematics (paspalum, c.330 spp.), and Aristida (threeawn, and evolution of this large, diverse, and phylogen- c.300 spp.); however, the monophyly of some etically advanced family are described in this of the genera is doubtful. Economically all the chapter. Agrostology is the science of grass classi- important cereal crops are grasses, including the fication, and, as noted by Gould (1955), is essential wheats (Triticum spp.), rice (Oryza sativa), maize to the study of grassland. However, the taxonomic (Zea mays), oats (Avena spp.), and barley (Hordeum treatment of the grasses has a fascinating history vulgare), sorghum (Sorghum spp.), millets (Panicum in itself as investigators moved from the use of pri- spp., Pennisetum spp.), and sugar cane (Saccharum mary morphological and anatomical characters to officinarum). Furthermore, grasses represent major include cytogenetic, physiological, and molecular sources of forage (see §4.2). characters allowing the development of increasingly A succinct description of the Poaceae provided evolutionarily informative classifications (Stebbins by the Grass Phylogeny Working Group (GPWG 1956). The evolution of this family, although still 2001) is as follows: incompletely understood, represents an interest- A monophyletic family recognizable by the following ing example of adaptation and co-evolution with synapomorphic characters: inflorescence highly brac- environmental and biotic factors, especially aridity teate. Perianth reduced or lacking. Pollen lacking scro- and grazing. biculi, but with intraexinous channels. Seed coat fused to inner ovary wall at maturity, forming a caryopsis. 2.1 Characteristics of the Poaceae Embryo highly differentiated with obvious leaves, shoot and root meristems, and lateral in position. Grasses are members of the family Poaceae, alter- A more extensive characterization of the Poaceae natively known as the Gramineae, within the Class is provided by Mabberley (1987), describing the Liliopsida (the monocotyledons) (Table 2.1). Within family as: the Liliopsida, the grasses are placed in the order Poales which includes 17 families including the Usually perennial and often rhizomatous herbs or (bam- closely related Joinvilleaceae, Ecdeiocoleaceae, and boos) woody and tree-like but without secondary
21 22 GRASSES AND GRASSLAND ECOLOGY thickening; cell-walls, especially epidermis strongly slits and nearly smooth pollen grains. Gynecium (2 (3 silicified, vessel-elements usually in all vegetative in Bambusoideae)), 1-locular with 2(3) stigmas, often organs; stems usually terete and with hollow internodes; large and feathery, ovule 1, orthotopous to almost ana- roots often with root-hairs but often with endomycor- tropous, (1)2-tegmic. Fruit (caryopsis) usually enclosed rhizae also. Leaves distichous (spirally arranged in e.g. in persistent lemma and palea, usually dry-indehiscent, Micraira), never 3-ranked, with usually open sheath and integuments adnate to pericarp, the seed rarely falling elongate lamina usually with basal meristem and pair free of these accessory structures such as when pericarp of basal auricles (narrowed to a petiolar base above becomes mucilaginous when wet and expelling the seed sheath in many bamboos); ligule usually adaxial at on drying out; embryo straight with well developed plu- junction of lamina and sheath, rarely 0. Flowers usu- mule covered by a closed cylindrical coleoptile, radicle ally wind-pollinated, usually bisexual, in 1–∞-flowered with a similar coleorhiza, and enlarged lateral cotyledon spikelets, spike-like to panicle-like secondary inflo- (scutellum), all peripheral to copious starchy endosperm rescences; spikelets usually with a pair of subopposite usually with proteinaceous tissue and sometimes also bracts (glumes) and 1-several distichous florets often on oily, rarely (Melocanna) absent. X 2 23. zig-zag rhachilla, the florets usually comprising a pair Additional details of some of these features are of sub-opposite subtending scale-like bracts (lemma and palea), 2 or 3 small lodicules (up to 6 in Bambusoideae). discussed in this chapter and Chapters 3 and 4. Anthers (1–)3 or 6 (especially Bambusoideae, where up to Members of the grass family are frequently 100 in Ochlandra), anthers elongate, basifixed but deeply confused with the superficially similar sedges sagittate so as to appear versatile, with longitundinal (Cyperaceae) and rushes (Juncaceae). However, a number of important features allow these families to be distinguished unambiguously even by the Table 2.1 Classifi cation of grasses non-expert (Table 2.2). Taxonomic level Name
Class Liliopsida (Monocotyledons) 2.2 Traditional vs modern views of Subclass Commelinidae grass classification Order Poales Because of the large size and great diversity of Family Poaceae (Gramineae) the family, it has proved difficult to produce a Type genus Poa (e.g., Poa pratensis L., Kentucky Bluegrass) systematic treatment of the grasses that is widely
Table 2.2 Features allowing the grasses (Poaceae) to be distinguished from the sedges (Cyperaceae) and rushes (Juncaceae). Note, exceptions occur for most character states listed. Also see Table 20.1 of Campbell and Kellogg (1986)
Characteristic Poaceae Cyperaceae Juncaceae
Leaves 2-(rarely 3-) ranked, flat, non-channelled 3-(rarely 2-) ranked, flat, channelled 2-many ranked, flat or terete Ligule Usually present Absent Absent Stem cross-section Terete (round), rarely compressed Triangular Terete Internodes Hollow or solid Solid Solid, with septae Inflorescence Spikelet (1 or more florets above the ‘Spikelet’ in racemes, panicles, Panicles, heads, corymbs, solitary glumes) in panicles, racemes, or spikes etc. Flowers/florets Floret (lemma, palea). Usually tiny 3-merous, chaffy, scales, or bristles; 3-merous, 6 scale-like perianth scales = lodicules = perianth inflated in Carex (perigynium) parts (‘drab lilies’) Stigma 2 (in frequently 3) 2–3 3 Anthers Attachment flexible (attached to filament Attached at the base, not flexible Attached at the base above the base) Fruits Caryopsis (grain), thin pericarp fused to Achene or nutlet, often lenticular or Loculicidal capsule seed coat (pericarp loose in Sporobolus) trigonous; style sometimes persistent Seeds 1 seeded 1 seeded Multiple seeded Habitat Mostly terrestrial Terrestrial and aquatic (emergent) Terrestrial and aquatic (emergent) SYSTEMATICS AND EVOLUTION 23 agreed upon or has remained stable for very long. Robert Brown (1810) was the first to understand As in other areas of systematics, molecular meth- the grass spikelet by recognizing it as a reduced ods have revolutionized the field (e.g. GPWG 2001; inflorescence branch. He also recognized the two Hodkinson et al. 2007b; Soreng and Davis 1998; great subdivisions of the Poaceae—the Panicoideae Zhang 2000). Understanding the systematics of and Pooideae subfamilies—describing the spike- grasses continues to be an active area of research. lets of each group, and their tropical–subtropical A brief history is given below. More detailed treat- vs cool-climate distribution and adaptations, ments can be found in Stebbins (1987), Watson (1990), respectively. Chapman (1996, Chapter 6), Clark et al. (1995) and In 1878 the English botanist George Bentham Soreng et al. (2007). Web-based electronic resources published a widely accepted natural classifica- for the family include: tion based on morphological characteristics of the inflor escence and fruit (Bentham 1878). He ● The World Grass Species Database (http://www. recognized 13 tribes within the Panicoideae and rbgkew.org.uk/data/grasses-db.html) Festucoideae (roughly equivalent to the Pooideae). ● Grass Genera of the World Database (http:// His classification scheme formed the basis for delta-intkey.com/grass) numerous later treatments of the grasses includ- ● Grass Manual on the Web (http://www. ing that of Bentham and Hooker (1883) and Bews’s herbarium.usu.edu/webmanual/) (1929, see Chapter 1) synopsis of the world’s ● Catalogue of New World Grasses (CNWG: http:// grasses. Hitchcock and Chase used Bentham’s mobot.mobot.org/W3T/search/nwgc.html) scheme in their 1935 and 1950 classification of US The use of grasses in agriculture and the nam- grasses in which 14 tribes in 2 subfamilies were ing of grasses extends back at least 2000 years. In recognized (Hitchcock and Chase 1950). Hitchcock ancient Greece, Theophrastus (370–287 bc) recog- and Chase’s classification was used as a standard nized in his Enquiry into Plants at least 19 different for treatments of North American grasses and grasses including what we now know as 2 bam- grasslands and was followed by most US floras boos (Bambusa and Dendrocalamus) and 3 species of up until the 1980s. wheat (Triticum aestivum, T. dicoccum, and T. mono- Up to this point, grass classification was based coccum) (Chapman 1996). Nevertheless, until the on the use of readily observable morphological fea- mid-eighteenth century the names of grasses were tures. In the 1920s and 30s the use of additional just compiled in lists without any taxonomic order. morphological, anatomical, cytological, and physi- For example, in 1708 Johann Scheuchzer published ological characters, often recognizable only from Agrostographiae Helvetica Prodromus, one of the first microscopic examination, heralded development papers dealing just with grasses. However, in 1753 of the ‘new taxonomy’. The taxonomic arrangement Carl Linnaeus in Species Plantarum provided the of genera based on these characters often differed starting point of a binomial nomenclature for flow- sharply from that based on traditional accepted ering plants. In Genera Plantarum (1767) he included homologies of characteristics of the inflorescence, more than 40 grass genera including many that and caused considerable changes in the focus of are well known and currently recognized such as the classical system (Stebbins 1956). Andropogon (bluestems), Panicum (panic grasses), The Russian cytologist N.P. Avdulov used chro- Hordeum (barley), and Poa. Of these, Panicum mosome studies, leaf anatomy, characteristics of was the most diverse genus with 23 binomials the first seedling leaf, organization of the resting described in Species Plantarum. However, his clas- nucleus, and starch grain characters to recognize sification was a sexual system based on numbers of the two ‘great’ subfamilies of the Panicoideae and floral parts, and hence highly artificial. Later clas- Pooideae (Avdulov 1931). In 1932 and 1936 the sifications of the flowering plants, including those Frenchman H. Prat used Avdulov’s characters, of the grasses, endeavoured to be natural, based traditional characters, and characters based on on assessments of adaptive radiations or character the leaf epidermis to recognize three subfamilies, homologies. extended in 1960 to six (Prat 1936). 24 GRASSES AND GRASSLAND ECOLOGY
Both Avdulov’s and Prat’s systems were phylo- taxonomic data. None of these classifications up to genetic, meaning that the groups recognized were this point were significantly influenced by DNA intended to be hierarchical and reflect the prevail- sequence data. ing knowledge of genetic and evolutionary history Among the recent floristic accounts of the within the family. The earlier morphologically grasses is that of the Flora North America based ‘natural’ classifications of Bentham were project (Barkworth et al. 2003, 2007, http://hua. natural in the sense that the groups reflected simi- huh. harvard.edu/FNA/;) with the subfamil- larities among the taxa, but not necessarily their ial classification based on analysis of molecular evolutionary history. The even earlier sexual clas- and morphological data by the Grass Phylogeny sification of Linnaeus, which was highly artificial, Working Group (GPWG 2000, 2001) and tribal placed often distantly related taxa in close prox- treatment of Clayton and Renvoize (1986, 1992, the imity because of the presence of shared number latter with only a couple of exceptions suggested of parts. Construction of phylogenetic systems, by the GPWG). The Flora of Australia and Flora although intellectually satisfying, may not be the of China projects similarly base their classifica- most convenient systems for purposes of identifi- tions of the Poaceae on the GPWG scheme (Flora of cation (Stebbins and Crampton 1961). Nevertheless, Australia 2002; Flora of China Editorial Committee all modern systems are evolutionary, intended to 2006). The GPWG classification was based on a reflect phylogeny. representative set of 62 grasses (0.6% of all grass One of the first to use the phylogenetic systems species and c.8% of the genera) plus 4 outgroup of Avdulov (1931) and Prat (1936) was English taxa. Six molecular sequence data sets (ndhF, rbcL, botanist C.E. Hubbard in his treatments of British rpoC2, phyB, ITS-II, and GBSSI or waxy), chloro- grasses (Hubbard 1954). Stebbins and Crampton plast restriction site data, and morphological data (1961), and later Gould and Shaw (1983) followed were used in a phylogenetic analysis that allowed suit with their treatment of the grasses of North a classification based on recognition of 11 previ- America. Both of these classifications recognized ously published subfamilies (Anomochlooideae, six subfamilies, including the long-recognized Pharoideae, Puelioideae, Bambusoideae, Panicoideae and Pooideae. Ehrhartoideae, Pooideae, Aristidoideae, Clayton and Renvoize (1986, 1992) published a Arundinoideae, Chloridoideae, Centothecoideae, phylogenetic treatment of grass genera arranged and Panicoideae) and the proposal of one new as 40 tribes in 6 subfamilies (Bambusoideae, subfamily (Danthonioideae) (GPWG 2001). Several Arundinoideae, Centothecoideae, Pooideae, subsequent analyses of molecular data (e.g. Davis Chloridoideae, and Panicoideae). Their treatment and Soreng 2007) have continued to improve the has been highly influential because, although systematic understanding of grass phylogeny traditional in the sense of presenting generic (Hodkinson et al. 2007b). descriptions and conventional keys, it was the first, detailed, worldwide, revision of grass gen- 2.3 Subfamily characteristics era and classification since Bews and Bentham. As such, it forms the basis of the most modern clas- Throughout the historical development of grass sification of the grasses. At about the same time, systematics, two large divisions of the family have Watson and Dallwitz (1988, 1992 onwards, http:// consistently been recognized: the subfamilies delta-intkey.com) published a computer database Panicoideae and Pooideae. These two subfamilies in DELTA (DEscription Language for TAxonomy) were first recognized by Robert Brown in 1810 describing 785 genera based on 496 characters in as the two primary subgroups of the Gramineae which initially 5 and then later 7 subfamilies were (as the Poaceae was then called). Bentham’s (1881) recognized. The search facility of the database treatment also recognized these subgroups as the allows character descriptions to be matched to tribes Panicaceae and Poaceae, respectively, as did unknown specimens and thus represented a major Hitchcock and Chase (1950). As noted above (§2.2), new development in the storage and retrieval of the ‘new taxonomy’ of the 1960s onwards expanded SYSTEMATICS AND EVOLUTION 25 the number of subfamilies as newly recognized GPWG (2001) and Kellogg (2002). Additional, groups were split out from the two larger groups. detailed descriptions of the subfamilies are pro- As described below (§2.4), the modern circumscrip- vided in Chapman (1996) and Chapman and Peat tion of 12 subfamilies (GPWG 2000, 2001) is expli- (1992), except that these sources use Clayton and citly phylogenetic and reflects division of the family Renvoize’s (1986) scheme in which five subfamilies into 2 main clades (monophyletic groups), the BEP were recognized. The ordering of the subfamily and PACCAD clades, with 2 subfamilies sister to descriptions provided below follows that depicted these main clades (Anonochlooideae, Pharoideae, in the cladogram proposed by the GPWG shown and Puelioideae) (Fig. 2.1). All the subfamilies in Fig. 2.1. recognized are well supported as monophyletic, The first three subfamilies—the Anomoch- except for Centothecoideae (GPWG 2001). The latter looideae, the Pharoideae, and the Puelioideae— is accommodated within the Panicoideae. are basal (early-diverging lineages) in the overall Poaceae cladogram (Fig. 2.1), with the Anomochlooideae being the earliest lineage to 2.3.1 Descriptions of subfamilies diverge among extant grasses. Two major clades The following subfamily descriptions are based are recognized, the BEP clade which includes the on the more extensive account provided by the Bambusoideae, Ehrhartoideae, and the Pooideae,
Dissarticulation below glumes
Three awns Panicoideae $ *
Centothecoideae $ * Diversification in Elongation of embryonic cooler climates mesocotyl internode Aristidoideae $ PACCAD clade Stamens reduced to three Danthonioideae * Radiation into open habitats Mid-tertiary diversification begins Arundinoideae * Multiflowered spikelets evolve Stigmas reduced to two Chloridoideae $* cpDNA: ndhF insertion Eriachneae $ Incertae sedis Spikelets and lodicules evolve Micraireae
Oldest known grass fossils, Pooideae * c.50–70 mya Arm cells evolve Ehrhartoideae * Seed coat fuses to ovary wall BEP clade Grass type embryo differentiates Perianth is reduced Streptogyneae cpDNA: rpoC2 insertion trnT inversion Radiation into forests Bambusoideae *
cpDNA: 6.4 kb inversion Puelioideae *
Pharoideae *
Anomochlooideae
Joinvilleaceae
Other Poales $ *
Figure 2.1 Summary phylogenetic tree of the grasses indicating significant morphological, ecological, and molecular (chloroplast DNA) events in the evolution of the family. The 12 subfamilies described in the text appear in boldface. Marked taxa: *, at least some included species have unisexual flowers/florets; $, at least some included species have a C4 carbon fixation pathway, Kranz anatomy, or both. Dark circles indicate nodes strongly supported by all data combined (bootstrap 99). Reproduced with permission of the Missouri Botanical Garden Press (GPWG 2001). 26 GRASSES AND GRASSLAND ECOLOGY and the PACCAD clade which includes the BEP clade Panicoideae, Arundinoideae, Centothecoideae, BEP is an acronym for the three subfamilies Chloridoideae, Aristidoideae, and Danthonioideae. included in this clade: the Bambusoideae, the
Ehrhartoideae, and the Pooideae. All are C3 Anomochlooideae grasses, but the Bambusoideae and Ehrhartoideae A small subfamily (four species among two genera: are generally most abundant in warm tropical Anomochloa marantoidea and Streptochaeta—three and subtropical regions whereas the Pooideae (the spp.) of perennial, rhizomatous herbs of shaded ‘cool-season’ grasses) are best represented in cool tropical forest understories. Presumed to possess and cold regions. the C3 photosynthetic pathway, these grasses lack grass-type spikelets; instead, the inflorescences Bambusoideae A large, ancient subfamily with (‘spikelet equivalents’) have complicated branch- c.1400 species of perennial (rarely annual), rhi- ing patterns and are comprised of bracts and are zomatous herbaceous or woody plants in 88 gen- one-flowered and bisexual. Basic chromosome era (including the genera Arundinaria, Bambusa, numbers: x 11 or 18. The presence of an adax- Ochlandra, and Pariana). Members of this subfamily ial ligule as a fringe of hairs is the single morpho- are found in temperate and tropical forests, tropical logical character supporting a monophyletic origin high montane grasslands, riverbanks, and some- of the subfamily. These grasses have no apparent times savannahs. The woody culms characterize economic value. many of the taxa in this subfamily and the familiar bamboos provide varied uses ranging from build- Pharoideae ing materials, scaffolding for high-rise buildings A subfamily with 12 species (including the genera (e.g. Gigantochloa laevis: Chapman 1996), garden Pharus and Leptaspis) of perennial, rhizomatous, canes, a food source (bamboo shoots), and in orna- monoecious herbs. Presumed to possess the C3 mental settings. Exclusively C3 plants, these grasses photosynthetic pathway, these grasses of shaded possess spicate, racemose, or paniculate inflores- tropical to warm temperate forest understories cences in which all of the bisexual (Bambuseae) or possess inverted (resupinate) leaf blades, and unisexual (Olyreae) spikelets of 1 to many florets paniculate inflorescences with unisexual, one- develop in one period of growth. Basic chromo- flowered spikelets. Basic chromosome number some numbers: x 7, 9, 10, 11, and 12. x 12. Members of this subfamily are of little for- age value (Harlan 1956). Ehrhartoideae (syn. Oryzoideae) A medium-sized subfamily with c.120 species including the genera Puelioideae Ehrharta, Leersia, Microlaena, Oryza, Potamophila, A poorly known subfamily with c.14 species (in and Zizania). Grasses in this subfamily are annual the genera Puelia and Guaduella) of broadleaved, or perennial, rhizomatous or stoloniferous, herba- perennial, rhizomatous herbs of shaded, African ceous to suffrutescent plants occurring in forests, rainforest understories. Presumed to posses the open hillsides, or aquatic habitats. Possessing the
C3 photosynthetic pathway, these grasses possess C3 photosynthetic pathway, these grasses possess racemose or paniculate inflorescences with sev- paniculate or racemose inflorescences with bisex- eral florets of which proximal florets are male, ual or unisexual spikelets including 0–2 sterile flo- with distal florets female or incomplete. Basic rets and 1 female-fertile floret. Basic chromosome chromosome number x 12. Traditionally classi- number x 12 (10 in Microlaena; 15 in Zizania). fied as bamboos, recent molecular analyses sup- Economically, this subfamily includes rice Oryza port the recognition of the two sister genera as sativa, American wild rice Zizania aquatica, and a an early-diverging branch within the Poaceae and problematic weed, the perennial Leersia hexandra. sister to the BEP and PACCAD clades (Clark et al. 2000). These grasses have no apparent economic Pooideae The largest subfamily with c.3560 species value. (including the genera Agrostis, Bromus, Diarrhena, SYSTEMATICS AND EVOLUTION 27
Elymus, Festuca, Lolium, Nardus, Poa, Stipa, and Sesleria) Andropogon, Panicum, and Saccharum) of annual of annual or perennial, herbaceous plants of cool or perennial, primarily herbaceous grasses of temperate and boreal regions, and high mountain the tropics and subtropics, but also in temperate regions of the tropics. Exclusively C3 plants, these regions. All the different photosynthetic pathways grasses possess spicate, racemose, or paniculate are represented (C3, C4 including PCK, NAD-ME, inflorescences in which the spikelets are predomi- and NADP-ME: see Chapter 4 for explanation of nantely bisexual, infrequently unisexual or mixed, C4 pathways) including some C3/C4 intermediates. including 1–many female-fertile florets, compressed Inflorescences are panicles, racemes of spikes, or a laterally. Basic chromosome numbers: x 7 (Bromeae, complex combination of these, with bisexual (uni- Triticeae, Poeae generally, few Brachypodieae), 2, 4, sexual in monoecious or dioecious members) spike- 5, 6, 8, 9, 10, 11, 12, 13. Economically, this large sub- lets frequently paired in long-short combinations family includes many important grasses (e.g. Lolium usually with 2 glumes, 1 sterile lemma, and 1 often perenne, Poa pratensis, and Schedonorus phoenix), orna- compressed female-fertile floret. Basic chromosome mental and amenity grasses (e.g. varieties of Briza, numbers: x 5, (7), 9, 10, (12), (14). Economically Deschampsia, and Festuca), and cereals (e.g. wheat, important plants include forage grasses, e.g. barley, oats, and rye). Panicum maximum (Guinea grass), Paspalum notatum (Bahai grass), and Pennisetum purpureum (elephant PACCAD clade grass), and some cereals (e.g. Echinochloa crus-galli A monophyletic clade including the Panicoideae, (Japanese millet), Panicum miliaceum (proso millet), Arundinoideae, Centothecoideae, Chloridoideae, Pennisetum glaucum (pearl millet), Sorghum bicolor, Aristidoideae, and Danthonioideae subfamilies. and Zea mays (maize). A number of major weeds The clade is strongly supported by molecular ana- are in this subfamily, including Digitaria sanguina- lysis; nevertheless, the only morphological charac- lis, Imperatra cylindrica, and Echinochloa crus-galli ter linking all the species is the presence of a long (when not planted as a crop). mesocotyl internode in the embryo (Kellogg 2002). For the most part, members of this clade grow in Arundinoideae A small subfamily, often treated as warm climates and/or flower late in the growing a ‘dustbin’ group for taxa of uncertain affinity, of season; hence they are often referred to as warm 33–38 species in 15 genera including Amphipogon, season grasses. Taxa of uncertain phylogenetic Arundo, Dregeochloa, Hakonechloa, Molinia, Moliniopsis, affinity (tribes Eriachneae, Micraireae, and genus and Phragmites). Eight of the genera from the Cyperochloa) were all left Incertae Sedis (GPWG 2001) crinipoid group (Crinipes, Dichaeteria, Elytrophorus, but were nevertheless placed in the PACCAD clade Letagrostis, Nematopoa, Piptophyllum, Styppeiochloa, on the basis of limited molecular evidence (Fig. 2.1). and Zenkeria) are only provisionally placed in this In support of earlier work by Pilger (1954, 1956 in group by the GPWG (2001). Recent analysis indi- Lazarides 1979), the Flora of North America and cates the presence of a monophyletic arundinoid the Flora of Australia projects both recently recog- core group, although this subfamily has often been nized the Micrairoideae as a subfamily (containing regarded as polyphyletic in a broad sense. Members the genera Micraira, Eriachne, Isachne, Pheidiochloa) of this subfamily are perennial (rarely annual), thereby expanding the PACCAD clade into the herbaceous to somewhat woody plants of temper- PACMCAD clade (Barkworth et al. 2007; Flora of ate and tropical areas. The reeds (Phragmites) are Australia 2005). However, these genera are often found in marshy habitats. Photosynthetic pathway represented in analyses with incomplete data and is C3. Inflorescences are usually paniculate with their true phylogenetic relationships with other bisexual florets of 2 glumes a sterile lemma and groups at the base of the PACCAD clade remain 1-several female-fertile florets. Basic chromosome uncertain (R. Soreng, personal communication). numbers: x 6, 9, 12. A number of economically useful grasses are included in this subfamily such Panicoideae One of the largest and best-recognized as Phragmites australis, common ‘reed’ used for subfamilies with c.3550 species (including thatching and screens (Chapman 1996) and Molinia 28 GRASSES AND GRASSLAND ECOLOGY caerulea (purple moor grass), which is bred as an and saline conditions, or high pH (Chapman 1996). ornamental. Arundo donax (giant cane), native in A number of range grasses of dry habitats are in Asia, is a problematic invasive (Table 1.8) following this subfamily including Astrebla spp. (Mitchel its escape from cultivation for use as an ornamen- grasses, Australia: Plate 8), Bouteloua dactyloides tal and screening plant. (buffalograss, North America), and Chloris gayana (Rhodesgrass, central Africa). Two members of Centothecoideae A small subfamily of 10–16 genera the subfamily are cereal grasses, Eragrostis tef (t’ef, with c.45 species (including Calderonella, Centotheca, Central Ethiopia), and Eleusine coracana (finger mil- Chasmanthium, and Thysanolaena) of annual or let, India, China, and Africa), and Astrebla lappa- perennial, herbaceous or reedlike, warm temper- cea is cultivated as fodder. Several Eragrostis spp. ate woodlands and tropical forest. Exclusively C3 are undesirable weeds (Watson and Dallwitz 1992 plants, these grasses are, for the most part, charac- onwards). terized by unusual leaf anatomy (e.g. palisade meso- phyll and laterally extended bundle sheath cells). Aristidoideae A small subfamily of c.350 species Inflorescences are racemose or paniculate with (including three genera: Aristida, Sartidia, and bisexual or unisexual (1–) 2–many-flowered spike- Stipagrostis) of annual or perennial, ceaspitose, lets often compressed laterally. Basic chromosome herbaceous grasses from mostly xerophytic tem- number: x 12. Members of this small subfamily perate to tropical zones, often in open habitats. have been historically placed in the Bambusoideae Photosynthetic pathways include C3 (Sartidia) and because of the superficial similarity to members of C4 (Aristida NADP-ME; Stipagrostis NAD-ME). this subfamily. There is no morphological synapo- Inflorescences are paniculate of spikelets with morphy that supports the subfamily as mono- bisexual florets including lemmas with three phyletic. Consequently, the circumscription of the awns, disarticulating above the glumes. Basic centothecoid clade itself remains uncertain and chromosome number: x 11, 12. In this subfamily based largely on molecular data (Sánchez-Ken and Aristida spp. and Sartidia spp. are of limited eco- Clark 2000). Unusual leaf anatomy characterizes nomic value and are frequently significant weeds most members of the subfamily, including the pres- of poor nutritional value and minor grazing value ence of palisade mesophyll and laterally extended in dry regions (e.g. Aristida dichotoma, A. longiseta, bundle sheath cells. Economically members of this A. oligantha which have awns that can damage live- subfamily are of limited value except Centhtotheca stock). Stipagrostis species are of value as cultivated lappacea which provides excellent fodder (Chapman fodder (S. ciliata, S. uniplumis) and as important 1996). Chasmanthium latifolium (Indian wood oats, native pasture species: e.g. S. ciliata, S. obtusa, S. plu- northern sea oats) is cultivated as an ornamental in mose (Watson and Dallwitz 1992 onwards). the USA where it is also native. Danthonioideae A small subfamily of c.300 spe- Chloridoideae A large subfamily of c.1400 species cies in 18–25 genera of perennial, occasionally including the widespread Chloris (c.55 spp.) and annual, herbaceous or rarely suffrutescent grasses. Eragrostis (c.350 spp.), of herbaceous (rarely woody) Members of this subfamily occur in mesic to xeric annuals and perennials of the dry tropics and sub- open habitats, mostly in the southern hemisphere tropics (some in temperate zones). Photosynthetic (Danthonia and Schismus are native in the north- pathway predominantly C4 (PCK, NAD-ME, except ern hemisphere). Photosynthetic pathway is C3.
NAD-ME in Pappophorum), although C3 in Eragrostis Inflorescences are paniculate or less commonly walteri and Merxmuellera rangei. Inflorescences racemose or spicate with bisexual or unisexual lat- are paniculate with spicate branches and usu- erally compressed spikelets with 1–6 (–20) female- ally bisexual spikelets of two glumes and 1–many fertile florets. The lemma includes a single awn. female-fertile florets, usually laterally compressed. Basic chromosome numbers: x 6, 7, 9. The pres- Basic chromosome numbers: x (7), (8), 9, 10. Many ence of haustorial synergids in the ovule, distant members of this family exhibit tolerance to drought styles, a ciliate ligule, a several flowered spikelet, SYSTEMATICS AND EVOLUTION 29 an embryo mesocotyl, and the absence of Kranz Some of the morphological changes associated anatomy and chloridoid microhairs are diagnostic with evolution of the grasses and the major groups features allowing the Danthonioideae to be distin- are summarized in Fig. 2.1. Some traits appear to guished from other subfamilies. Members of this have evolved once, such as the early and acceler- subfamily have limited economic value although ated development of the embryo relative to seed Danthonia spicata is used as a poor-quality forage and fruit maturation. Several leaves, a vascular grass in North America, Pentaschistis borussica is an system, and organized shoot and root apical mer- important native pasture species in Africa, as are istems are produced in the grass embryo (Kellogg Schimus arabicus and S. barbatus in Euroasia. 2000). This feature separates the grasses from the Joinvilleaceae and Ecdeiocoleaceae (their nearest 2.4 Fossil history and evolution relatives) and all other monocots (see §2.4.1). Other traits have evolved more than once, such as C4 pho- The phylogenetic picture that emerges from the tosynthesis which is exclusive, in the grasses, to recent rbcl sequence analyses is that the Poaceae several closely related subfamilies of the PACCAD are monophyletic with a Cretaceous origin 83–89 clade (Kellogg 2000) (Chapter 4). Complicating the Ma (million years ago) (Janssen and Bremer 2004; issue are a large number of apparent reversals, Michelangeli et al. 2003). The Anomochlooideae such as the apparent regaining of pseudopetioles represents the earliest-diverging extant lineage in the Bambusoideae and some members of the (GPWG 2001). The next diverging lineage is the PACCAD clade, and the regaining, three or four Pharoideae, followed by the Puelioideae. The rest times, of the inner whorl of stamens within the of the grasses are believed to form a clade, with bambusoid/ehrhartoid clade (GPWG 2001). In the the BEP and PACCAD clades forming two major absence of knowledge of the underlying genetics monophyletic groups (Fig. 2.1). The origin of the of these traits, it is also possible that these changes BEP and PACCAD clades is unclear and may have really represent retained primitive characters, or been as early as 55 Ma, certainly no later than the the evolution of superficially similar, but novel, Late Eocene (34 Ma) (Prasad et al. 2005; Strömberg characters. 2005). Viewed as a whole, the BEP PACCAD clade includes the majority of grass species and is sup- 2.4.1 The Joinvilleaceae and Ecdeiocoleaceae ported as monophyletic by six morphological connection synapomorphies (shared unique ancestral traits): loss of the pseudopetiole, reduction to two lodicules, Early workers (e.g. Engler 1892, and see review in loss of the inner whorl of stamens, loss of arm and Cronquist 1981) assumed the grasses and sedges fusoid cells, loss of lamina on the first seedling leaf (Cyperaceae) to be closely related and placed them (Bambusoideae and Orzyeae only), and evolution of into the Glumiflorae or Cyperales, on the basis of unisexual florets (most lineages) (GPWG 2001). The floral reduction and biochemistry. Such a close phylogenetic patterns within and between the BEP relationship between these two groups is not and PACCAD clades are uncertain and unclear. now believed. In 1956, Stebbins suggested that the Part of the problem lies in a bias of sampled taxa grasses were evolutionarily close to the most primi- from the northern hemisphere, and the lack of sam- tive Liliaceae such as members of the Flagellariaceae pling in general (Hodkinson et al. 2007a). Much of and Restionaceae. The Flagellariaceae (one genus, the evolutionary action may have taken place across Flagellaria, of four species) are small old-world the Gondwanan continent. The extensive radiation tropical herbs with grass-like leaves with tendril- and diversification may have been too rapid to like tips, whereas the Restionaceae are a mostly allow clear resolution of phylogenetic pattern with southern hemisphere family (38 genera of 400 spe- the data currently available (Kellogg 2000) although cies) that mostly lack leaf blades, but appear to take phytolith assemblages indicate diversification of the the place of grasses in some areas of South Africa chloridoids within the PACCAD clade by at least and Australia. In the Cape region alone there 19 Ma (Strömberg 2005). are 10 endemic genera and 180 endemic species 30 GRASSES AND GRASSLAND ECOLOGY
(Mabberley 1987). Later, Dahlgren et al. (1985) and account for these distributions are (1) long-distance Stebbins (1987) suggested that the grasses may, in dispersal across the Atlantic and Indian Oceans, or fact, be closest to the Joinvilleaceae, a small fam- (2) radiation across a continuous Gondwanan equa- ily that was only recognized in 1970, consisting of torial continent followed by subsequent isolation a single genus (Joinvillea) comprising two species and further evolution. Phytolith evidence (see §2.4.3) (J. ascendens and J. bryanii) limited in their distri- is consistent with the view that the divergence and bution to western Malaya and the Pacific islands. spread of the BEP and PACCAD clades occurred With long, narrow leaves with open sheathing across Gondwana before the biogeographic separa- bases, unbranched and hollow stems, and bisex- tion of the Indian subcontinent from the rest of Asia ual flowers of six scale- or bract-like perianth seg- by c.80 Ma (Prasad et al. 2005). However, the paucity ments each, the plants bear a superficial similarity of grasses in the early Tertiary or late Cretaceous to some grasses (Heywood 1978). Nevertheless, the fossil record (see below) does not help in resolving Joinvilleaceae is an isolated group of obscure ori- this issue (Hodkinson et al. 2007b). gins. Recent analyses (GPWG 2001; Hodkinson et al. 2007a and references therein; Michelangeli et al. 2.4.3 Fossil history 2003) place the Joinvilleaceae and Ecdeiocoleaceae as sister groups and the closest living relatives to The early fossil record of the grasses is poor. Grass- the grasses, with an obscure and uncertain rela- like leaves and putative floral structures have been tionship to the Restionales and Cyperales (Fig. 2.1). observed in late Cretaceous sediments. For exam- The gain of multicellular microhairs is a structural ple, Cornet and colleagues (Cornet 2002) recovered synapomorphy supporting the sister relation- fossils of grass-like leaves with paniculate inflores- ship between the Joinvilliaceae and the grasses cences and grass-like flowers from the Turonian– (Michelangeli et al. 2003). The presence of a 6.4 kb Raritan Upper Cretaceous (90 Ma) clays in New inversion in the chloroplast DNA genome, and the Jersey, USA. Included with these fossils were pla- occurrence of long–short cell alternations in files tanaceous leaves (plane tree family), ericaceous of cells adjacent to stomatal files in the leaf epi- leaves (heather family), and possible lauraceous dermis, are synapomorphies previously used to leaves (laurel family). Many of these plants may join this clade (Kellogg 2000), which have recently have grown on delta levees and overbank deposits, been shown to join the Joinvilliaceae–grass clade close to the site of deposition. Other sediments from with the Ecdeiocoleaceae (a family of two genera, the site indicate that the depositional environment Ecdeiocolea and Georgeantha, often included in the was a coastal plain forest of pines (Prepinus sp., Restoniaceae) (Michelangeli et al. 2003). The short Pinus sp.) and angiosperm trees (Dewalquea spp., cells go on to make stomata or silica bodies. The Platanaceae) along with the achlorophyllous sapro- common ancestor of these groups presumably phytic Mabelia connatifila—the oldest unequivocal evolved both of these characters. fossil monocot from the Upper Cretaceous 90 Ma (Gandolfo et al. 2002). Some of the earliest fossil grass remains are of 2.4.2 Biogeographic origin pollen grains, which are of limited value because It is unclear where the grasses evolved. The cur- of their ultrastructural uniformity. Monoporate rent distribution of the early-diverging lineages of pollen assumed to be fossil Poaceae is placed into grasses presents a fragmented picture. The basal one of several form genera including Graminidites, Anomochlooideae are restricted to South and Monoporoites, and Monoporopollenites (Macphail and Central America, the Pharoideae are pantropical, Hill 2002). However, confident assignment of these and the Puelioideae are found only in tropical Africa. fossils to the Poaceae requires the observation of Furthermore, of the sister families, Joinvilleaceae minute channels or holes penetrating the outer occur on Borneo, New Caledonia, and Pacific islands pollen wall (Kellogg 2001). The oldest confirmed (e.g. Hawaii) and Ecdeiocoleaceae are limited to records of grass pollen are from the Paleocene south-west Australia. Two possibilities that would (55–65 Ma) of South America and Africa. Reports of SYSTEMATICS AND EVOLUTION 31 older Late Cretaceous Masstriichtian-age grass or grass-relative fossil pollen grains cannot be attrib- uted unambiguously to the Poaceae. The earli est recorded grass pollen from North America is from the uppermost Eocene (Graminidites gramineoides). Grass pollen becomes abundant thereafter in the succeeding Oligocene and Miocene. The earliest accepted fossil records of the grasses are phytoliths (silicified plant tissues: see §4.4) pre- served in Late Cretaceous (Maastrichtian) titano- saurid dinosaur coprolites from central India Figure 2.2 The oldest macrofossil of a grass. A spikelet with two (Prasad et al. 2005). These fossils include morpho- florets with glumes (g) is visible. Bar = 1 mm. Reproduced with types attributable to at least five taxa of grasses permission from Crepet and Feldman (1991). within the [Bambusoideae Ehrhartoideae] and PACCAD or Pooideae clades. The taxonomic diversity of these phytolith morphotypes sug- found in association with mammalian hair pre- gests an evolution, diversification, and spread of served in amber from the late Early Miocene–early basal Poaceae 65–71 Ma in Gondwana before India Middle Miocene (15–20 Ma) (Iturralde-Vinent and became geographically isolated. MacPhee 1996; Poinar and Columbus 1992). Hooked The earliest evidence of mega (macro)-fossils con- hairs on the lemma provide the earliest evidence firmed as grasses is from the Eocene Wilcox forma- for dispersal via attachment to animal fur (epizoo- tion (c.54 Ma) of western Tennessee, USA (Crepet chory). Assignment of the fossil to a modern-day and Feldman 1991). These sediments contain mac- extant genus is further support for the idea that rofossils of spikelets, inflorescence fragments, diversification of the grass family had occurred quite leaves, and whole plants. The fossils reveal spike- a bit earlier than indicated in the fossil record. By lets with two florets subtended by two alternate, the time the following Oligocene epoch (34–23 Ma) slightly unequal, keeled glumes. Three exserted ended, it is quite clear from the fossil record that stamens per floret are present, with dorsifixed grasses representing several separate extant tribes anthers (Fig. 2.2). However, the bracts are poorly and genera were present. By the late Miocene preserved and it is possible that there is only one (7–5 Ma) there is evidence that grasses possessing floret with six stamens (Soreng and Davis 1998). the C4 photosynthetic pathway had evolved (§2.4.4 Vegetative remains reveal small, perennial plants and Chapter 4). Thomasson et al. (1986) described with leaves arising from a rhizome. These and other fossil leaves with ‘chloridoid’ Kranz anatomy, typi- features preserved in the pollen support the diag- cal of C4 grasses. How much earlier than this the nosis that these plants fit clearly within the Poaceae C4 pathway evolved is unknown, although there sensu lato. In the absence of additional diagnostic is speculation that biochemical precursors of C4 characters, the subfamily affinity of these fossils is photosynthesis may have existed as far back as the uncertain although the authors suggested similar- Permo-Carboniferous (Osborne and Beerling 2006). ities with the Pooideae or Arundinoideae—both C3 subfamilies. Nevertheless, these fossils represent 2.4.4 Ecological origin of grasses and the earliest clear evidence of grasses, and of wind- grasslands: relationship to arid conditions pollinated herbaceous monocots. Furthermore, the and rise of grazing mammals well-defined nature of these plants (their affin- ities, although uncertain, do not suggest a primi- The original grasses evolved in deep shade or for- tive grass) is consistent with an Upper Cretaceous est margins, characteristics retained by the extant origin of the family. Anomochloa, Streptochaeta, Pharus, Puelia, Guaduella, The second-oldest grass macrofossil is a female the bamboos, and the basal pooid Brachyelytrum. spikelet of the extant genus Pharus (Bambusoideae) Little diversification of the grasses occurred in 32 GRASSES AND GRASSLAND ECOLOGY
these habitats for millions of years. Major diversifi- ● diurnal shifts in temperature and moisture → cation is associated with spread into open habitats scale-like perianth, and fleshy lodicules that open in the mid-Miocene (Kellogg 2001). and close easily. The spread of grasses and their subsequent evo- The extent to which any of the changes described lution is believed to reflect climatic factors to a large above reflects true adaptation to aridity or a extent. For example, current distribution of the co-evolutionary relationship with grazers, one in Andropogoneae tribe (in Panicoideae) shows a close which both partners reciprocally adapt to each relationship with tropical areas of high midsum- other over time, is uncertain and contentious. It mer rainfall (Hartley 1958). The C Panicoideae and 4 is uncertain whether traits presumed to relate to Chloridoideae dominate tropical and subtropical drought and grazing tolerance are truly beneficial grasslands. On a narrower taxonomic basis, differ- (aptations), incidentally beneficial (exaptations), or entiation of the genus Poa is closely tied to regions the result of selection to confer the present benefit of high latitude and high altitude. In the USA, Poa (adaptation). Although climatic factors have prob- spp. form more than 5% of the grass flora in areas ably played a large part in the evolution of the of cool summer temperatures, i.e. areas below the grasses and the spread of grasslands, the poten- 24 °C midsummer (July) isotherm (Hartley 1961). tially co-evolutionary relationship with grazing Climatically, the diversification of grasses and the mammals has been the subject of much conjecture spread of grasslands coincides with increased arid- and speculation (Coughenour 1985). Certainly, evo- ity, especially during the Oligocene (34–23 Ma). In lutionary change in grazing animals, specifically North America, for example, the Rocky Mountain ungulates (hoofed mammals) appears to track uplift led to aridity of the Great Plains causing a the climatically driven development of extensive retreat of the forests in the late Oligocene and savannahs and grasslands from the mid-Miocene Miocene (23–5.3 Ma) (Coughenour 1985). In Africa, onwards. increased continental elevation led to increased The grasses arose in the late Cretaceous–early aridity, also during the Oligocene, allowing the Tertiary, but they diversified and spread into large spread of grasslands. vegetation formations in the mid-late Miocene Thus, grasses were able to spread during periods (12–5.3 Ma). The first appearance of extensive, open of increased aridity because of the possession of a grasslands varied worldwide. In North America number of traits adapted for drought; these include it was towards the end of the Miocene (8–5 Ma) basal meristems, small stature, high shoot density, (Axelrod 1985) (Fig. 2.3), although savannah or deciduous shoots, below-ground nutrient reserves, short-sod grasslands appear to have arisen in the and rapid transpiration and growth (Coughenour early Miocene (c.19.2 Ma) (Strömberg 2004). In South 1985). The basic scenario postulated by Stebbins America, grass-dominated ecosystems may have (1987) included the following selection pressures arisen as early as the Eocene–Oligocene boundary and associated adaptations by grasses driving (34 Ma) (Jacobs et al. 1999). By contrast, in central their evolution: and western Europe the grasslands today are sec- ● trampling by large herbivores → heavy sympo- ondarily anthropogenic and arose from farming dial rhizome system and pastoralism following the spread of Neolithic ● grazing → basal leaf meristems husbandary in the Holocene (Bredenkamp et al. ● grazing by hypsodont ungulates and/or phy- 2002). The modern North American tallgrass prai- tophagous insects → silificiation of epidermal rie is also of recent origin following the retreat of cells woodland during the warm, dry hypsothermal ● open conditions of savannahs → wind period c.4000 years ago. pollination The rise of grass-dominated ecosystems was
● wind pollination → condensation of compound probably preceded by the evolution of the C4 racemes → racemes of spikelets, more intense pol- photosynthetic pathway in the middle Miocene len clouds, increased target for pollen (or perhaps even earlier in the Oligocene) under SYSTEMATICS AND EVOLUTION 33
North South America Eurasia America Africa Australia O Ma Pliocene
Earliest exclusive C4 diet
Earliest floral evidence for grass-dominated ecosystems Miocene Earliest C4 isotopic evidence Dentition adapted to grazing
25 Ma Oligocene
Eocene
Earliest grass pollen 50 Ma Earliest grass macrofossil
Paleocene
Figure 2.3 Generalized summary of the establishment of grass-dominated ecosystems worldwide. Reproduced with permission of the Missouri Botanical Garden Press from Jacobs et al. (1999).
conditions of low atmospheric partial pressure of alternating with a fire-susceptible dry season. Fire
CO2 (the CO2-starvation hypothesis; see §4.1). At an in the dry season inhibits and kills trees and cre- earlier date, dentition adapted to grazing appeared ates a high-light environment also favouring C4 (i.e. hypsodont, high-crowned, cheek teeth) (Jacobs grasses. Moreover, increased frequency and sever- et al. 1999). The finding of grass phytoliths in late ity of drought conditions again favours C4 grasses Cretaceous dinosaur coprolites (see §2.4.3) is evi- at the expense of woody vegetation. This combi- dence that grasses were part of their diet. Late nation of climatic conditions created a novel envi-
Cretaceous Gondwanatherian mammals pos- ronment allowing the expansion of C4-dominated sessed hypsodont cheek teeth and could have eaten grassland. A predictable and frequent fire regime grasses too, suggesting the possibility of an even allowed the grasslands to be maintained. earlier co-evolutionary interaction between grasses The extent to which grass evolution is a conse- and vertebrate herbivores than previously thought quence of adaptation to herbivory is unclear. For (Piperno and Hans-Dieter 2005). example, siliceous phytoliths in grass epidermal
The rapid and global spread of C4-dominated cells can be viewed as an adaptation of grasses grassland in the late Miocene (5–8 Ma) was at to herbivory (the abrasive silica wearing down the expense of woodland and reflects changes the teeth, thus providing a grazing deterrent). in the climate conducive to frequent fire (Keeley Conversely, the evolution of hypsodonty may be a and Rundel 2005) including increased seasonal- response to increased siliceous grass in the diet, or, ity of rainfall (Osborne 2008). Increased seasonal- evolution of both herbivores and grasses may have ity would have allowed high production (i.e. fuel) been reciprocal. Phytoliths recovered from sedi- during warm, monsoon-like, moist conditions ments indicate a C3-dominated grassland in the 34 GRASSES AND GRASSLAND ECOLOGY
North American Great Plains in the early Miocene to running in open country such as grassland. (25 Ma), at least 7 × 106 years before adaptations of As the grasslands expanded through the Pliocene, horses in the Great Plains to grasslands (Strömberg the now-extinct single-toed ancestor of the mod- 2002, 2004). Conversely, other hypsodont ungu- ern horse, Pliohippus, became more widespread. lates, such as oreodonts and camels, occurred in At the same time, the three-toed Hiparion and the Great Plains during the Eocene (55–34 Ma), Neohipparium diminished in abundance as wood- well before the Miocene. Tying the story even land areas decreased. A hoof with three toes is closer together, anomalously high species rich- adapted to dodging sideways as well as running ness of browsing ungulates in the mid-Miocene forwards: more necessary in a woodland than a (c.18–12 Ma) woodland savannah of North America grassland. is postulated to be the result of elevated levels of In summary, the major phases in the evolution primary productivity, itself a consequence of per- of grasses and grasslands are (Jacobs et al. 1999) haps higher-than-present levels of atmospheric (Fig. 2.3):
CO2 (Janis et al. 2004). As these climatic conditions ● changed and grasslands spread, the numbers of origin of Poaceae in forest margins or shade dur- browsing species decreased. ing Cretaceous ● The evolution of horses is pertinent (Chapman opening of forested environments in early to 1996). The genus Equus, which includes the mod- middle Tertiary ● increase in abundance of C grasses in middle ern horse (E. caballlus), the wild ass (E. hemionus), 3 the African ass (E. africanus), and the zebras Tertiary ● origin of C grasses in middle Miocene (probably (E. burchellii, E. zebra, and E. grevyi), is the sole 4 remaining genus of an evolutionary lineage in the earlier) ● spread of C -grass-dominated ecosystems at the Equidae that included several now-extinct mem- 4 expense of C grassland and/or woodland in the bers. Derived from five-toed mammals, the mod- 3 ern horse is single-toed; an adaptation well suited late Miocene. CHAPTER 3 Ecological morphology and anatomy
Perhaps the season when the sight of the green meadows 3.1 Developmental morphology— most delights us, is early spring. How beautiful are they, the phytomer as the sunlight comes down upon their gleaming blades, and the blue heavens are hanging over them! Central to the understanding of grass morphology Anne Pratt, The Flowering Plants, Grasses, and growth is the phytomer concept (Moore and Sedges, and Ferns of Great Britain, and their Moser 1995). This posits that the phytomer, consist- allies the Club Mosses, Pepperworts and ing of an internode and node together with the leaf Horsetails (1873) blade and sheath at the upper end, and an axillary bud at the lower end, is the fundamental growth Since, in general, increase in xerophytism has every- unit of a grass (Briske and Derner 1998; Gould and where meant evolutionary advance, all these vegetative Shaw 1983). A single phytomer matures from top features are a very useful guide towards an understand- to bottom (blade, sheath, internode). A stack of ing of the main evolutionary trends. phytomers (i.e. a shoot) matures from bottom to top. (Bews 1929) The oldest phytomer is at the bottom of the stack, with the longest leaf to protect the growing point; The common possession of a number of charac- the youngest phytomer at the top of the stack has teristic morphological features makes grasses only a short leaf that affords less protection. A grass readily recognizable to even the lay person— plant thus consists of a collection of ramets (clonally although, as noted in Chapter 2, there is often produced parts capable of potentially independent confusion with other similar families such as existence: Silvertown and Lovett Doust 1993), each the rushes (Juncaceae) and sedges (Cyperaceae). of which is a repeated series of phytomers succes- In this chapter the morphology and anatomy of sively differentiated from individual apical meris- a grass plant is described, with mention where tems (Briske and Derner 1998). A tiller (a secondary appropriate of the ecological relevance and impor- stem) is a collection of phytomers differentiated tance of the different features. A number of other from a single apical meristem (Moore and Moser sources can be consulted for additional details 1995). Morphological variation within and among such as Metcalf (1960), Langer (1972), Chapman grasses is a consequence of variation in the number (1996), Gould and Shaw (1983), or Renvoize (2002) and size of ramets that themselves comprise a as well as electronic databases (see § 2.2) includ- number of phytomers. This variation encompasses ing Watson and Dallwitz (1992 onwards). There is diminutive grasses such as Poa annua through arbo- considerable diversity in form and function that real giants such as Dendrocalamus spp. amongst the relates to the evolutionary adaptation of grasses bamboos that can grow up to 40 m (Metcalf 1960). to their environment. In general, the trends in Quantification of the variation among phytomers in grass evolution reflect a series of adaptive reduc- a single grass plant can provide a basis for under- tions in size, complexity, and number—albeit standing morphogenetic and environmental con- with notable exceptions and a number of revers- straints on plant development (Boe et al. 2000). For als (Stebbins 1982). example, in the perennial prairie grass Andropogon
35 36 GRASSES AND GRASSLAND ECOLOGY gerardii, blade length, blade weight, and sheath weight decrease among phytomers of the main culm in acropetal fashion, whereas sheath length Node Spikelets can remain constant. Meristematic, or growth, tissue in grasses is located immediately above the nodes in the stems, Blade and at the base of the leaf blade. Because the basal nodes of perennial grasses tend to be short, and the apical meristem is borne close to the ground envel- Blade Sheath oped by protective leaf sheaths, grasses are well adapted for rapid regrowth following grazing.
Ligule 3.2 Structure of the common oat Avena sativa Node The common oat provides a useful starting point for understanding the morphology of a typical grass plant (Fig. 3.1). The main parts to note above ground are the culm, the leaves, and the flower head. The culm is the grass stem and consists of Culm Panicle several cylindrical tubes of unequal length closed at the joints by solid tissue. The joints, or nodes, are generally a darker colour. The hollow portions of the stem between the nodes are the internodes. The leaves of grasses are borne in two rows, alternating on opposite sides of the culm. The leaf LI consists of three portions: the blade, sheath, and ligule. The blade is the upper flattened portion; Figure 3.1 Common oat Avena sativa, × 0.5. LI: detail showing the sheath is cylindrical embracing the culm, open base of leaf blade and ligule. Reproduced with permission from along one side with one margin overlapping the Hubbard (1984). other (in A. sativa at least). The ligule is a thin membrane that occurs at the junction of the sheath and the blade. The flower head terminates the culm and (FL) is composed of three parts, a pair of small consists of a main axis plus several spreading scales (lodicules, LO), three stamens, and a pistil. branches or pedicels. Spikelets are borne at the The pistil consists of a single ovary, with a single tips of the pedicels. In A. sativa, the flower head ovule, plus two feathery styles. When fertilized, is a panicle by virtue of the spreading branches. the ovule develops into the grain. Spikelets (S on Fig. 3.2) consist of several scales, It should be emphasized that the structure of alternatively borne in two rows on opposite sides Avena sativa described above represents a ‘typical’ of a short stem, the rachilla. The spikelet is the grass, and there is extensive variation among basic reproductive unit in grasses, historically species, described below, that both forms the basis forming the basis for classification (Chapter 2). of classification (Chapter 2) and reflects adaptation Each spikelet is subtended by two outer scales, to the environment. the glumes (G1, G2), which envelop the spikelet. In A. sativa, there are 2–3 florets per spikelet. Each 3.3 Culms floret (FS) consists of an outer scale, the lemma (L), and an inner scale, the palea (P). The lemma has The vegetative shoot apex of a grass contains the a short extension at the end, an awn. The flower apical or terminal meristem at its tip and is usually ECOLOGICAL MORPHOLOGY AND ANATOMY 37
CE CH roots, at the nodes. Rhizomes are common in many perennial grasses and may contain substantial amounts of storage tissue. Branching of the culm is either sympodial or LO monopodial. Sympodial branching occurs where there is successive development of lateral buds, just behind the apex. The main axis stops growing in this P case. Conversely, monopodial branching occurs when the culm increases in length by division of the apical meristem, with branching by lateral FS L branches occurring in acropetal succession (Usher S 1966). Culms with aerial stems branching exten- sively at the base produce a caespitose (clumped or tufted) habit (e.g. Schizachyrium scoparium, Festuca ovina, Koeleria macrantha), whereas branching in the upper culm produces a shrubby appearance (e.g. Andropogon glomeratus). Thus, culms can be erect to decumbent, creeping, shrubby, or even treelike. Most commonly, the shoot tip of lateral branches emerges from the apex of the enclosing leaf sheath (i.e. intravaginally) producing the caes- pitose habit, although the more diffuse stolonifer- ous or rhizomatous architecture of sod grasses (e.g. Festuca rubra) develops when the shoot tip breaks G 1 through the sheath (i.e. extravaginally). Rhizomes FL G2 and stolons can both branch and produce adven- titious roots at the nodes that can be especially Figure 3.2 Spikelet of common oat Avena sativa, FL, LO, × 6; important in allowing vegetative reproduction or rest × 2. CE, grain (abaxial view showing embryo); CH, grain persistence if the plant is fragmented. Microstegium (adaxial view showing hilum); FL, flower; FS, floret; G1 and G2, glumes; L, lemma; LO, lodicules; P, palea; S, spikelet. Reproduced vimineum, for example, is an annual grass, invasive with permission from Hubbard (1984). in North America, which produces extensively branched prostrate culms that root freely at the nodes (Gibson et al. 2002). Rhizomes and stolons can integrade in some species, e.g. Cynodon dactylon located close to the ground protected by envelop- (Fig. 3.3). ing leaf sheaf bases. Shoots originate either from The production of secondary (or branch) shoots the seed embryo (the primary shoot) or from veg- from axillary buds can be important in the growth etative buds (axillary buds) in a leaf axil of an older and population persistence of grasses. For example, shoot (secondary shoots or tillers). Thus, culms Digitaria californica, a dominant perennial grass in may branch to form a compound shoot system. the semi-desert ranges of the USA, possesses axil- The location and extent of branching and ramet lary buds on most internodes of the culm, except the development largely determines the physical struc- panicle internode. The current year’s crop of basal ture of the grass plant (Fig. 3.3). Stolons are above- culms are produced in the spring or summer from ground branches that tend to run prostrate over axillary buds (Cable 1971). The importance of axil- the soil surface (e.g. Agrostis stolonifera), whereas lary buds for population persistence was demon- below-ground branched stems are referred to as strated in Bouteloua curtipendula and Hilaria belangeri rhizomes (e.g. Poa rhizomata). Both structures pos- in semi-arid oak–juniper savannah, in Texas, USA sess leaf buds and (at least, vestigial or scale) leaves, (Hendrickson and Briske 1997). Dormant axillary can branch, and may give rise to aerial stems, and buds attached to the base of reproductive parental 38 GRASSES AND GRASSLAND ECOLOGY
Blade Auricle Collar Ligule
E Sheath
Spikelet
Blade D Stolon Culm Rhizome
Stolon Sheath C Node
B A
Rhizome Fibrous roots
Figure 3.3 Structure and architecture of the grass plant: A, general habit (Bromus unioloides); B, rhizomes; C, stolon; D, rhizome and stolon integradation (Cynodon dactylon); and E, leaf at junction of sheath and blade, showing adaxial (left) and abaxial (right) surface. Reproduced with permission from Gould and Shaw (1983). tillers remained viable for 18–24 months, exceeding 3–7 genets m–2 yr–1 (Suzuki et al. 1999). Clonal parental tiller longevity by 12 months. These buds development of caespitose grasses depends on thus provide a meristematic source for tiller recruit- ramet production and death rate, with clones ment into populations that exceeds the longevity of showing a developmental sequence of pre- the seed bank of many perennial grasses (see § 5.1.4). reproductive, reproductive, and post-reproductive Perennial grasses in which ramets are replaced stages of 5–10, 15–30, and 15–25 years to complete, annually can live for many years, with some esti- respectively (Gatsuk et al. 1980). Deschampsia ceas- mates of longevity exceeding 1000 years (Briske pitosa clones in northern Europe, for example, die and Derner 1998). Making age determinations or back in the centre during the mature reproduc- estimates of genet natality (births) in an organ- tive stage, with the whole clone fragmenting in ism that is continuously growing and senescing the post- reproductive phase (Fig. 3.4). The clonal is difficult, but has been aided by the develop- fragments of old genets (plants arising as indi- ment of DNA-based molecular marker techniques. viduals from a seed; Gibson 2002) are free-living For example, randomly amplified polymorphic and capable of producing new ramets, but they DNA (RAPD) methods (Gibson 2002) were used may be short-lived, contributing little to popula- to estimate genet natality of Festuca rubra at tion maintenance (Briske and Derner 1998). The ECOLOGICAL MORPHOLOGY AND ANATOMY 39
A
B
Pre-reproductive Reproductive Post-reproductive
Figure 3.4 Schematic showing architectural development of Deschampsia caespitosa clones in northern Europe. A, aerial view; B, side view. 35–60 years is required for clones to grow from seedlings to senescence, note the development of hollow crowns in the reproductive phase followed by clonal fragmentation in the post-reproductive phase. Reproduced with permission from Briske and Derner (1998) redrawn from Gatsuk et al (1980).
physiological integration conferred among ramets ● net absolute TAR (NTAR): of clonal grasses is discussed in Chapter 4. N N Tillers are aerial axillary shoots, consisting NTAR ————2 1 of a culm and its associated leaves. Tillering is t2 t1 the production of new tillers. Intravaginal tillers where N is the number of live tillers (per plant, grow up between the leaf sheaths, and extrav- 1 pot, unit area) at time t and N is the number of aginal tillers burst through the enclosing sheath 1 2 live tillers at time t (Thomas 1980). If N N bases or arise from buds not enclosed by existing 2 2 1 (number of new tillers produced between t and t ) sheaths. Tufted or casepitose grasses exhibit intra- 1 2 then the expression gives the gross TAR. vaginal tillers, whereas the production of stolons (e.g. Poa trivialis) or rhizomes (e.g. Elytrigia repens) ● proportional PAR (PTAR): is through extravaginal tillers. Aerial tillers can 1 N − N arise from the nodes of extended stems. For exam- PTAR = —– × ———–2 1 ple, the annual grass Microstegium vimineum pro- N1 t2 − t1 duces aerial tillers as it grows through the season where net and gross rates can be calculated (Gibson et al. 2002). depending upon how N is determined, as with Much agricultural and ecological research has 2 absolute TAR. been devoted to understanding and quantifying tiller dynamics. Some of the basic calculations Net and gross tiller death rates can be estimated made to quantify tiller dynamics include tiller in a similar manner by measuring the rate of appearance rate (TAR)—the rate at which tillers ‘appearance’ of dead tillers (e.g. Hendon and Briske become apparent to the eye (of course, they form 1997). earlier). The most frequent forms of TAR that are Tiller appearance rates for the caespitose grass calculated include: Arrhenatherum elatius are illustrated in Fig. 3.5. 40 GRASSES AND GRASSLAND ECOLOGY
400(a) Tiller dynamics 300
200
100
0
–100 Number of tillers Cumulative births –200 Cumulative deaths Total alive –300 Flowering tillers × 10 Birth month of flowering tillers × 10 –400 (b) Tiller appearance rate 3 NTAR PTAR × 100
2
1
0 Tillers per day Tillers
–1
–2
–3
Nov Dec Feb Mar Apr May June July Aug Sept Oct Oct 1981 Jan 1982 Date
Figure 3.5 Tiller dynamics of Arrhenatherum elatius, Newborough Warren, Anglesey, UK (Gibson, unpublished): (a) Seasonal tiller flux; (b) tiller appearance rates. Tiller births were obtained from 25 cm2 plots placed in the centre of five tussocks. NTAR, net tiller appearance rate (tillers d–1); PTAR, proportional tiller appearance rate (tiller d–1).
For both NTAR and PTAR, values >0 reflect There is continuous tiller death, but it was most growth of the grass clumps in terms of tiller pronounced during the summer and the accom- numbers, and values <0 indicate a decrease in the panying decrease in tiller births at this time led tiller population. For A. elatius, the figures indi- to a sharp decline in the population numbers of cate that clumps were growing from September living tillers. In the dune grassland where this through May, and experienced negative growth grass was growing, it was the dominant spe- (tiller loss) during the summer. This seasonal flux cies and the seasonal tiller dynamics influenced in tiller numbers is also illustrated in the plot the rest of the plant community (Gibson 1988a, of cumulative tiller births and deaths (Fig. 3.5). 1988c). ECOLOGICAL MORPHOLOGY AND ANATOMY 41
Similarly, in the cool-season perennial Schedonorus the red:far red ratio is typically associated with the phoenix new tillers are produced throughout the year, shade effect of leaf canopies. especially in the late winter to early spring, and after ● Soil moisture affects tillering, with drought flowering in late summer (Gibson and Newman reducing tiller production, reducing tiller size 2001). Tiller mortality is highest in June because of and the percentage of reproductive tillers, and intraclonal competition among tillers. By contrast, increasing mortality rate. For example, in a lightly complete winter dieback of tillers is typical for most grazed Schizachyrium scoparium pasture a mean of warm season perennial grasses. For example, across 51 tillers plant–1 during a year with above average much of its range in the US Great Plains, the warm- precipitation was reduced to a mean of 26 tillers season perennial Schizachyrium scoparium dies back plant–1 in a drought year (Butler and Briske 1988). in the late autumn (i.e. complete tiller mortality), Whereas 20% of the tillers were reproductive in the with new tillers emerging in late spring through wet year, there were zero reproductive tillers in the summer. However, in Texas, in the southern part of drought year. its range, a few tillers on the periphery of clumps ● Mineral nutrition status of the soil and hence can persist from one growing season to the next of the plant is important for tiller production. (Butler and Briske 1988). Tillering increases with increased supply of nitro- The tillers form a hierarchy with a few large gen, phosphorus, and potassium. Nitrogen is the tillers and lots of small ones, many of which are most important of these, and interacts with phos- repressed. Tillering is under genetic control but phorus and potassium; at low nitrogen, tillering is is highly modified by the environment since it suppressed even with additional phosphorus or requires intense meristematic activity and cell potassium. The response to fertilizer in the field enlargement; both processes requiring energy and depends on nutrients in the soil and the develop- resources. An increase in tillering stimulates leaf mental stage of the plant. production and growth leading to an increase in ● Grazing, although causing mortality of plant parts total leaf area per plant. The following general directly affected, can stimulate tillering through affects of the environment on tiller production release of buds in the axis of leaf bases on the stem. have been observed (Langer 1972): For example, continuous grazing of Schedonorus phoenix by sheep increased the number of tillers ● Tillering is temperature sensitive, with an inhi- while reducing leaf extension rates (Mazzanti et al. bition of tillering at high temperatures related to 1994). By contrast, grazing-sensitive species exhibit respiration rates and soluble carbohydrate content declines in tiller production and hence total tiller of the plant. Warm conditions at night appear to numbers with herbivory. Sensitivity to herbivory be more deleterious than warm days. Temperate can depend upon the timing of defoliation; for species have relatively low optimum tempera- example, defoliation of Eriochloa sericea during tures for tillering: 18–24 °C in Lolium perenne and pre-culm and post-culm stages displayed greater 10–25 °C in Dactylis glomerata (Langer 1972). By cumulative tiller mortality (28% and 11%, respec- contrast, tillering in subtropical species increases tively) compared to undefoliated plants (39% and up to 35 °C. 21%, respectively) (Hendon and Briske 1997). ● Light interacts with temperature and high light intensity favours tiller production. The current In some sense grass plants can be regarded rather than past light intensity is the most important, as a population of tillers, just as trees have been as plants repressed in shade resume tillering when described as a population of buds (Jones 1985). brought back out into the light. Light quality can Tiller life history is dependent on the life history of affect tiller dynamics. Experimentally increasing the species and the environmental conditions and the red:far red ratio enhanced spring tiller produc- season. Tillers may be born and die after only a few tion in Sporobolus indicus and Paspalum dilatatum, weeks remaining vegetative throughout their life, and increased tiller death for both species during or they can persist vegetatively from one season the autumn (Deregibus et al. 1985). An increase in to the next or longer. Ultimately if a tiller does 42 GRASSES AND GRASSLAND ECOLOGY become reproductive then it dies after flowering long-shoot growth (e.g. Andropogon gerardii) can is complete. In Arrhenatherum elatius we noted ear- occur with few phytomers; early elongation of the lier the seasonal flux in tiller dynamics (Fig. 3.5). inflorescence uses most of the phytomers, leaving In addition, there is distinct seasonality in tiller few phytomers at the base. Thus, with few axillary survivorship (Fig. 3.6). Tiller production increases buds there is only minimal tillering. rapidly following flowering late in the summer, and Specialized rhizome development occurs in most of the tillers born in the autumn overwinter the bamboos through the production of extensive and live into the early summer. By contrast, till- jointed, segmented rhizomes. Lignification of the ers born in early summer live only one or two ground tissue makes the rhizomes strong and months. Arrhenatherum elatius flowered from July rigid. Rhizome development in bamboos takes to October (Fig. 3.6). Tillers that flowered were born one of two forms. Pachymorph rhizomes are short from November the year before through June, but and thick, pear-shaped, with lateral buds giving 60% of them were born from February to April. rise only to rhizomes and culms arising only from An understanding of culm growth is best related the apex of the upturned rhizome; this gives rise to phytomer production (§ 3.1). For example, short- to densely clumped bamboos, e.g. Bambusa spp. By shoot growth (e.g. Bouteloua gracilis) is a conse- contrast, leptomorph rhizomes of ‘running bam- quence of many phytomers. Late elongation of the boos’ are long and slender with every node bear- inflorescence uses only a few phytomers, leaving ing a shoot bud and roots. The rhizome tip grows many phytomers at the base, each with axillary continuously forward through the soil allowing buds (a stack of phytomers), which then can elon- the plant to form sometimes massive clonal colo- gate to produce more growth (tillering). Conversely, nies that can cover entire hillsides, e.g. Phyllostachys
Arrhenatherum elatius tiller survivorship
100
10 Log 10% tiller survivorship
1
Nov Dec Feb Mar Apr May June July Aug Sept Oct Oct 1981 Jan 1982 Date
Figure 3.6 Survivorship of Arrhenatherum elatius tillers, Newborough Warren, Anglesey, UK (Gibson, unpublished). Newborn tillers were marked the first week of each month from October 1981 to October 1982 in 25 cm2 plots placed in the centre of five tussocks. Each line represents a different tiller cohort. ECOLOGICAL MORPHOLOGY AND ANATOMY 43 nigra which forms dense forests in the rain forest exception is vegetative prolifery (also called pro- of east Maui, Hawaii. Rhizome cuttings from both liferation, but only incorrectly, vivipary) that can pachymorph and leptomorph species allow easy occur as in Festuca viviparoidea (viviperous sheep’s propagation so long as some buds and culms are fescue) where a branched reproductive inflores- attached to the cutting. cence can revert to vegetative growth (Stace 1991). In addition to the architectural function of In this situation the spikelet above the glumes branching and vegetative reproduction, rhizomes is converted into a leafy shoot (Clark and Fisher act as storage organs for grasses. Sugars and 1986). Proliferation has been reported in Agrostis, starches can occur in large amounts, and support Deschampsia, Eragrostis, Festuca, Oryza, Phleum, Poa, initial growth in the spring and regrowth follow- Setaria, Sorghum, and Zea. ing grazing. For example, when total non-structural The switch to flowering is terminal for mono- carbohydrate concentration in the rhizomes of carpic plants (dying after one fruiting season), Sorghum halepense was experimentally reduced by whether annual grasses or semelparous (once- 60%, regrowth from the rhizomes was not possible. flowering) perennials. Many genera have both Grass rhizomes have been used for human con- annual and perennial members, e.g. the brome sumption; for example, rhizomes of Phragmites aus- grasses with the annual Bromus japonicus and tralis are sometimes eaten or processed for starch B. tectorum, and the perennial B. inermis among by native people in Tasmania (Australian National others. Many bamboos are long-lived and mono- Botanic Gardens 1998). carpic, often flowering simultaneously over large Other storage or vegetative reproduction organs areas at intervals of 100 years or more before include bulbs and corms which may be developed dying. For example, there are 35 species of Sasa at the base of culms. True bulbs are rare, but occur in in Japan all of which show these characteris- Poa bulbosa, whereas corms (or corm-like swellings) tics (Makita 1998). Whether a perennial plant is occur in several genera, including Poa, Melica, monocarpic or polycarpic (fruiting many times), Molinia, Colpodium, Arrhenatherum, Beckmannia, the individual reproductive shoot is monocarpic Hordeum, Phleum, Ehrharta, and Panicum (Clark and dying after reproduction is complete. Fisher 1986). The corms (haplocorms of Evans 1946) The nature of the inflorescence is described are fleshy swellings at the base of stems, and can be in § 3.6. particularly important in vegetative reproduction. In Arrhenatherum elatius var. bulbosum, the corms 3.4 Leaves occur in a string of four or five basal internodes, each up to 1 cm broad with a regenerative bud Leaves develop from primordia in the dermatogen that can germinate. As with rhizomes, the food and hypodermis (outer cell layer) on the flanks of the reserves in these structures can be important in the conical apical dome of the stem. Leaf primordia are diet of animals. Yellow babbons (Papio cynocepha- initially entirely meristematic (possessing ability lus), for example, will dig up and eat the corms for cell division), but meristematic activity becomes of Sporobolus rangi in the Amboseli region of East limited to an intercalary region which includes the Africa (Amboseli Baboon Research Project 2001). ligule on the inner (adaxial) face and the leaf lam- Flowering culms arise when the apex of a vegeta- ina abaxially. The location of the intercalary meris- tive culm increases its growth rate and initiates the tem means that leaves can continue to grow if the inflorescence. Internodes elongate and, typically, tip of the lamina is removed, e.g. through grazing the flowering stem grows as an erect structure. Leaf or mowing. Stems are usually short so leaves arise primordia are formed rapidly on the elongating close together. The leaves are arranged on alternate stem apex, and buds in the axil of these primordia sides of the apex leading to distichous phyllotaxy, grow rapidly. Leaf growth is inhibited and bud i.e. the leaves are arranged in two vertical rows. growth ensues as they become spikelet primor- Spiral phyllotaxy in grasses is extremely rare, but dia. With respect to a single stem, this change in occurs in members of the Australian genus Micraira function of the apical meristem is permanent. An (Watson and Dallwitz 1988). 44 GRASSES AND GRASSLAND ECOLOGY
The grass leaf consists structurally of three parts; short cells occurring in rows, in pairs, or singly, the blade (lamina), the sheath, and the ligule. The and possessing a silica body (phytolith). The size first leaf of a culm branch or lateral shoot consists and shape of silica bodies varies with taxa, and of a membraneous, modified sheath structure, their presence in sediments is used to reconstruct lacking a blade, known as the prophyll or pro- the evolution of grassland ecosystems (Strömberg phyllum. This structure protects the immature lat- 2004). Silica causes the teeth of grazers to wear eral stem axis by being initially tightly appressed down (Chapter 4) and its presence has been impli- to it. Subsequent leaves include a blade with the cated in the co-evolution of grasses and herbivores lamina emerging from the shoot rolled or folded (Chapter 2). Stomata occur in the intercostal zone on about the midrib. The lamina is normally linear or the adaxial and abaxial surfaces alternating in files lanceolate, with characteristic parallel nerves, nar- with the oblong intercostal cells, and vary in size row relative to its length, elongate, laminate, and from 15 to 50 µm with their appearance depend- flat (capable of being flattened if rolled). Leaves ing on the shape of the subsidiary cells. Surface can be stiff, setaceous, needle-like, or acicular (per- features associated with the epidermis include manently inrolled—e.g. Miscanthidium teretifolium papillae on the long cells (Bambusooideae) or lin- which has a blade that is almost cylindrical with the ing grooves, rare glandular hairs (Pappophoreae adaxial surface recognized only by a small groove). tribe in the Chloridoideae), and one- or two-celled Leaf margins are entire, smooth, or scabrous. In microhairs and prickle hairs (common and wide- some species the margins are so strongly scrabrous spread throughout the Poaceae). that the grass has become well known for its ability The leaf sheath is the basal part of the leaf. It to cut the skin, e.g. rice cutgrass (Leersia oryzoides). is interpreted as a flattened petiole, and affords In size, grass leaves range from the diminutive protection to the shoot and developing branches Monanthocloë littoralis with blades usually <1 cm to within. Clasping the stem, leaf sheaths occur the large Neurolepis nobilis (bamboo) with blades up either with their free margins overlapping, or, to 4.5 m long and 30 cm wide. infrequently, their margins fused (connate) to Leaf shape is related to environmental condi- form a tube (e.g. Glyceria, Festuca, Bromus). The tions. In the humid tropics grass leaves are often leaf sheath frequently has a distinct midrib that large, often with ovate or oblong blades. By con- extends into the blade. At the top of the sheath trast, in semi-arid regions they are often narrow and at the base of blade on the abaxial surface is and linear, becoming involute (inrolled) under a collar which can be a petiole-like contraction, as drought conditions. Cladoraphis spinosa, a grass of in most bamboos. Modifications of the leaf sheath deserts in the western Karroo (South Africa), is include husks around the ear of maize (Zea mays). an extreme example of xeromorphic adaptation Sometimes (rarely) the sheath and blade are not in which the linear- lanceolate to lanceolate leaf clearly differentiated, e.g. Neostapfia colusana, blades are hard, woody, and needle-like, up to a tufted Californian annual, and Orcuttia spp. only 6 mm wide and rolled (Watson and Dallwitz (Gould and Shaw 1983). 1988). The ligule is a taxonomically diagnostic fea- Epidermal features of leaves often reflect adap- ture. Occurring on the adaxial surface at the tations to xeric conditions—e.g. bulliform cells at apex of sheath, the ligule varies widely in tex- base of furrows (grooves) between the vascular ture, size, and shape (Fig. 3.7) (additional abaxial bundles (i.e. in the intercostal zone) on the adaxial ligules occur in, for example, Bambusa forbesii). surface allow the leaf to inroll in drought (protect- Commonly membraneous (Bambusooideae, ing stomata). Bulliform cells are found, for example, Ehrhartoideae, Pharoideae, and Pooideae), white or in the leaves of the fine-leaved fescues (e.g. Festuca brownish, the ligule can be a stiffened membrane ovina), and in marram grass Ammophilla arenaria (e.g. Sorghastrum nutans), a ciliate fringe of hairs that grows on often-droughty coastal sand dunes. (Aristidoideae, Arundinoideae [except Arundo], and Another characteristic feature of the epidermis of Danthonioideae [exceptions are Monachather and grass leaves is the presence of silica cells. These are Elytrophorus]) (Renvoize 2002), or absent (Neostapfia, ECOLOGICAL MORPHOLOGY AND ANATOMY 45
plasts in membraneous ligules containing starch grains indicates a photosynthetic function. The presence of rough endoplasmic reticulum, numer- ous mitochondria, hypertrophid dictyosomes and associated vesicles, and paramural bodies in the cells of membraneous ligules suggest a secretory role. The secretion of extracellular products may act 3 1 2 as a lubricant to assist the exsertion of the enclosed leaf or culm (Chaffey 2000). Leaves are usually similar among different shoots. However, scale leaves occuring on stolons and rhizomes are generally relatively small, pale green in colour, and non-photosynthetic. In bam- boos there is a progressive elaboration of leaf shape on successive nodes up a culm. In these grasses the lower leaves have only a leaf sheath that provides 5 4 little photosynthetic contribution to the plant. Further up, the lamina becomes well developed, and effectively photosynthesizes. The change from one leaf type to another up the stem can be gradual or clear cut (e.g. Sasa) (Chapman 1996). Leaves are produced continually while the tiller is alive or until a culm switches over to the production of an inflorescence. There is thus a continuous turnover of leaves with new leaves 6 8 on a tiller expanding as older, lower leaves die. In 7 Schedonorus phoenix, for example, there is a flush of Figure 3.7 Ligules and auricles at junction of leaf sheath and new leaf production in the spring, with a new leaf blade (× 5). 1, Phleum bertolonii; 2, Bromus sterilis; 3, Melica emerging when the lamina of its predecessor on uniflora; 4, Schedonorus pratensis; 5, Schedonorus phoenix; a tiller has fully expanded (Gibson and Newman 6, Alopecurus pratensis; 7, Sieglingia decumbens; 8, Anthoxanthum 2001). Leaf expansion continues until the ligule odoratum. Reproduced with permission from Hubbard (1984). emerges. Leaf longevity is a cost-benefit issue to a grass, as it is for other plants, in which leaf lifespan Orcuttia) (Chaffey 2000). The type of ligule is usually is a balance between the costs of construction and uniform within a genus, but in Panicum both types maintenance, and the benefits accrued through occur among the different species. Ear-like projec- carbon gain (Kikuzawa and Ackerly 1999). The tions of tissue called auricles can occur at the junc- youngest upper-culm leaves are physiologically tion of the sheath and the blade (e.g. Schedonorus the most active; the older, lower leaves, which may phoenix) or there can be a tuft of hairs here (several be shaded by the upper leaves, photosynthesize at Eragrostis spp). The role of the ligule is unclear but low rates (Skeel and Gibson 1998). Reported leaf it has been viewed as some sort of aerial root cap. lifespan or longevity ranges from 31 ± 1.4 days The passive hypothesis suggests that it acts to pre- in Bouteloua gracilis (Craine and Reich 2001) to vent water, dust, and harmful spores and insects 25 months in Oryzopsis asperifolia (McEwen 1962). In from reaching the tender parts of the sheath and the latter report, O. asperifolia leaves are recorded as developing culm (Chaffey 1994; Chaffey 2000). The overwintering and remaining green throughout. active hypothesis suggests that the ligule has an Leaf longevity also varies depending when in a additional physiological role. Although they lack season a leaf is produced, as early-season leaves stomata, the presence of well-developed chloro- may senesce by late summer. Photosynthesis, leaf 46 GRASSES AND GRASSLAND ECOLOGY respiration, leaf nitrogen concentrations, and spe- (Weaver 1919, 1920). Later, Weaver and Darland cific leaf area are all positively correlated among (1949a) developed the monolith method in which a one another and negatively correlated with leaf block of soil is removed from the field and water is longevity (Reich et al. 1997). Leaf longevity appears used to gently separate soil from the roots. The pic- to be determined at least in part by nitrogen sup- ture that emerged from these studies of the North ply rates and therefore can be altered greatly by American prairie (Weaver and Darland 1949b) was plant feedback to the cycle (§ 7.2). Sodium fertilizer one of a complex and dynamic system with as increases leaf longevity in Lolium perenne, princi- much niche differentiation below ground as above pally as a result of decreased leaf senescence rather (Fig. 3.8). The grass roots were observed to form a than increased leaf production (Chiy and Phillips dense mass penetrating the soil column entirely,
1999). C3 grasses were observed to show a moder- deep into parent materials. Most of the roots are ate increase in leaf longevity under elevated CO2 located in the upper soil layers; for example, 43% compared with C4 grasses which showed no such of the root system by weight of Andropogon gerar- increase (Craine and Reich 2001). This difference is dii occurred in the top 10 cm, with 78% in the top attributable to the physiological difference among C3 30 cm (Weaver and Darland 1949b). Roots of neigh- and C4 grasses and the relationship between carbon bouring plants intermixed thoroughly in the upper gain and nitrogen cycling (Chapter 4). Significant soil. Weaver (1961) noted, for example, the manner decreases in leaf lifespan and increases in leaf in which roots of the caespitose Sporobolus heter- production were observed along a Mediterranean olepis extended outward from the crown occupying old-field succession sequence (Navas et al. 2003). the soil between widely spaced bunches. These changes were partly due to differences in More recently, ecologists have developed an life forms among stages; for example, the increase array of non-destructive and less invasive meth- in leaf production recorded was explained by the ods to examine root activity including the use of replacement of therophytes (annuals, e.g. Aegilops radioactive and non-radioactive tracers, rhizotrons geniculata, Brachypodium distachyon), occurring only with root windows and minirhizotrons making in the earliest successional stage, by hemicrypto- use of laser optics (Böhm 1979; de Kroon and Visser phytes (perennials, e.g. Brachypodium phoenicoides, 2003; Smit et al. 2000). Bromus erectus) in the later stages. Grass roots at maturity are wholly adventitious and fibrous. Seminal roots, which are the first roots to grow in a seedling (see § 3.7), function 3.5 Roots for only a short period of time, but during their More than 60% of the living biomass of grasslands short life appear to absorb more nutrients per unit is below ground. Estimates of below-ground peak weight than the adventitious roots (Langer 1972). biomass across a range of tallgrass prairie sites When the seminal roots die they are replaced by ranged from 700 to 2100 g m–2 in the top 90 cm adventitious roots, which consist of a primary root of soil (Rice et al. 1998). Generally, the extent of plus 2–7 first-order branches. The primary root may the root system is correlated with above-ground be indistinguishable from other roots and does growth. Root:shoot ratios range from 0.7:1 to 4:1 not resemble the familiar tap root of many her- with range grasses mostly between 0.8:1 and 1.5:1 baceous dicots. In tufted grasses the adventitious (Gould and Shaw 1983). The proportion of biomass roots arise from basal nodes of the main axis, and allocated below ground varies among species and from nodes on stolons, rhizomes, and tillers near with environmental conditions. Generally, the pro- the ground: i.e. any node in contact with the soil portion of plant biomass below ground decreases can develop roots. Roots developing from nodes with increasing soil moisture (Marshall 1977). develop from leaf bases and push through the sub- Consequently, ecologists need to make a special tending leaf sheath. Whorls of adventitious roots effort to understand this part of the system. Early can arise from nodes above elongated internodes researchers laboriously dug pits and trenches in up to 1.5 m above ground, e.g. the prop or buttress the ground, endeavouring to trace grassland roots roots of Sorghum spp. ECOLOGICAL MORPHOLOGY AND ANATOMY 47
1 2 7 5 6 3
4
1
2
3
4
5
Figure 3.8 Below-ground niche separation of 6 root systems in the North American prairie. 1 and 7, Schizachyrium scoparium; 2, Psoralidium tenuiflorum; 3 and 5, Koeleria macrantha; 4, Astragalus crassicarpus; 6, 7 Brickellia eupatorioides var eupatorioides. Note that the grasses place their roots at different levels, whereas the forbs extend much deeper. Scale is in feet. Reproduced 8 with permission from Weaver and Fitzpatrick (1934).
With little dominance of any main axis (except trichoblasts—cells which grow less rapidly then as a seedling), the topology of grass root systems other epidermal cells that are not going to become is diffuse. Whereas other plants exhibit a topo- root hair cells. Root hairs are responsible for water logical response to limiting resources, grasses and nutrient uptake. The density of root hairs appear to show little variation in root diameter can be related to mycorrhizal status (Chapter 5, (usually <5 mm in diameter) at different branch- Tawaraya 2003), soil pH (Balsberg and Anna 1995), ing levels (Robinson et al. 2003). Nevertheless, and texture (Bailey 1997). perhaps because of the diffuse nature of grass root systems, the fine root mass is higher and 3.5.1 Distribution of roots in fine root length greater in temperate grasslands soil and turnover than in any other biome (1.5 kg m–2, 112 km m–2, respectively) (Robinson et al. 2003). Per unit of Root biomass, production, and disappearance fluc- root mass, temperate grasslands have far more tuate seasonally. Biomass increases through the fine roots than any other system (fine/total root growing season with adequate soil water. The top mass ratio = 1.0). 10 cm of the soil is the most dynamic and sensi- Root hairs cover long lengths of the root epi- tive to environmental conditions with respect to dermis, unlike in dicots in which root hairs are root growth (Rice et al. 1998). Root growth has been limited to the area behind the root tip. The root shown to decline towards the end of the growing hairs are long and persistent, developing from season, not because of decreasing soil temperature, 48 GRASSES AND GRASSLAND ECOLOGY but, in the tundra grass Dupontia fisheri, because of reduction in light intensity on Bromus inermis led to decreasing daylength (Shaver and Billings 1977). a 30-fold decrease in root weight compared with Environmental factors including fire, graz- only a 5-fold decrease in shoot weight. ing, temperature, and nutrients affect root pro- Root production follows a seasonal pattern. duction and turnover. Root biomass is generally Under Lolium perenne/Trifolium repens (ryegrass/ higher under frequent burning, and this is related clover) swards, new adventitious roots were to higher rates of root production, not decreased produced through late winter to early spring, with senescence (Rice et al. 1998). Grazing produces a var- the rate falling off in April or May to a low rate iable response of the grass root system (Milchunas during the summer (Garwood 1967). Differences and Lauenroth 1993). In a global comparison of among four grasses in these grasslands (two cul- 236 grassland sites, root biomass was unrelated tivars of L. perenne, Dactylis glomerata, and Phleum to species compositional differences associated pratense) were minimal. More adventitious roots with grazing. However, positive effects of graz- were produced in February–April than at any other ing occurred in 61% of sites where grazing had a time of the year. These roots did not branch imme- positive effect on annual net primary productiv- diately and elongated slowly at first, but some of ity. At the local scale, root systems of Schizachyrium them continued growth in the lower soil horizons scoparium were observed to deteriorate, decreas- until midsummer. The roots produced in the late ing in density, under increased grazing intensity summer lived only a few days and failed to pen- (Weaver 1950). The intensity of clipping, used as etrate to any great depth in the soil. By contrast, an experimental surrogate for grazing, has been some of the September–November roots lived and shown to be inversely related to root production grew through the winter into the following spring (Branson 1956). Indeed, in the latter study, which and summer. The general pattern of a summer was conducted on five US range grasses (Pascopyrum decline in root production has been observed in smithii, Pseudoroegneria spicata, Hesperostipa comata, several species (Huang and Liu 2003; Murphy et al. Poa pratensis, and Bouteloua gracilis) clipping effects 1994). The roots of annual grasses do not normally, showed a more pronounced effect on the root sys- of course, live for more than a year. However, tem than the above-ground system. This suggests winter annuals, which germinate in the autumn, that under heavy grazing, effects would be exhib- rapidly grow numerous roots following germina- ited below ground before they were apparent above tion that overwinter becoming well developed in ground. Above-ground tissue removal, especially time for spring growth. The roots of the annual if in excess of 50%, can cause root growth to stop Bromus tectorum (cheatgrass), for example, can pen- for a period of time, presumably as the plant goes etrate to >30 cm deep in the soil by mid-November, through a period of resource conservation while eventually reaching 1.2–1.5 m below the surface foliage tissues are restored (Crider 1955; Jameson (Hulbert 1955). 1963). The loss of roots after clipping is most rapid As indicated above, much of the root system of near the root tips. perennial grasses dies and is replaced each year; Supplemental nutrients in the short term cause 50% in Poa pratensis and Agrostis capillaris (Sprague an increase in root biomass, but in the long term 1933). Root turnover, i.e. the net result of produc- the response may be different (Rice et al. 1998). The tion of new roots and disappearance of old ones, is amount and depth of soil moisture is more impor- high in drought conditions; e.g. root turnover was tant than nutrients. Shallow soil moisture leads to 564% during a drought year in US tallgrass prai- shallow root systems, and with deep soil moisture rie, compared with 389% the following year when the roots go deeper. The distribution of root weight there was adequate rain. Globally, root turnover in the soil column and the total amount of roots in grasslands increases exponentially with mean vary with soil type, particularly with respect to annual temperature (Gill and Jackson 2000). Root permeability (Weaver and Darland 1949b). Light turnover rates for temperate grasslands range from intensity incident on above-ground leaves affects 0.83 yr–1 in the central Netherlands to no annual root growth. Langer (1972) describes how an 18-fold turnover in US shortgrass steppe, with an overall ECOLOGICAL MORPHOLOGY AND ANATOMY 49 mean of 0.47 yr–1 (Lauenroth and Gill 2003). In or pedicelled spikelets on the inflorescence axis tropical grasslands, by contrast, mean root turno- or in simple or compound branching systems. ver is 0.87 yr–1, and in high-latitude (mostly tundra) Terminal spikelets mature first and the basal ones grasslands turnover is 0.29 yr–1. Many individual last. As in many things, Zea mays is an exception; roots stay alive for more than 2 years. The follow- maturation in the pistillate inflorescence ear of ing percentages of main adventitious root axes corn begins in the middle proceeding up and were observed to survive for two growing seasons: down the ear. Koeleria macrantha, 30%; Hesperostipa spartea, 57%; There are three main types of inflorescence Schizachyrium scoparium, 23%; Andropogon gerardii, (Plate 2); the panicle, the raceme, and the spike, 45%; Bouteloua curtipendula, 36%; and Sorghastrum although this categorization represents extremes nutans, 37% (Weaver and Zink 1945). of a continuum.
● In a panicle, spikelets are borne on stalks (pedi- 3.6 Inflorescence and the spikelet cels) on primary, secondary, even sometimes tertiary, branches arising from the main axis. The The inflorescence is the flowering portion of the inflorescence is a panicle in most grasses, e.g. shoot (Fig. 3.1). It is delimited at the base by a Panicum, and the panicle represents the original culm node bearing the uppermost leaf. There are form of inflorescence in grasses. The branching pat- normally no leaves within the inflorescence itself. tern in a panicle may be loose (e.g. Avena, Bromus, The upper culm leaf is usually reduced in blade Calamagrostis, Eragrostis, Panicum, Poa), or contracted, length compared with other leaves, but the sheath narrow, cylindrical, and dense (i.e. contracted as in may be enlarged and envelops the developing inflo- Phleum, Alopecurus, Phalaris, Lycurus). Spikelets can rescence. In some grasses, the mature inflorescence be sessile or short-pedicelled along primary inflo- remains within or partially within the sheath (e.g. rescence branches, and can be digitate at the culm Microstegium vimineum, Sporobolus compositus). apex or distributed along the main inflorescence There is tremendous variation in inflorescence axis; e.g. all members of the Chlorideae tribe, and morphology among grass genera and species, many genera in the Paniceae and Andropogoneae. and this variation forms the basis of classifica- ● In a raceme, spikelets are stalked on pedicels tion (Chapter 2). The variation described below is directly on the main axis. The inflorescence can be constant mostly within a species. The bamboos have reduced to a single terminal spikelet as in Danthonia atypical inflorescences, including florets arranged unispicata. Some grasses such as Echinochloa spp. in pseudospikelets, glumes with the potential for and Paspalum spp. have a paniculate inflorescence psuedospikelet formation or subtended by bracts with racemose branches. and/or prophylls, and atypically large numbers of ● In a spike, the spikelets are all seated on the floral parts (e.g. 4–6 glumes in Nastus) (Table 4.1 in main inflorescence axis itself—there are no stalks. Chapman 1996). Spikelets may be solitary at the nodes, e.g. Lolium, Inflorescences are generally borne above ground Triticum, Agropyron, or two or more per node, e.g. on erect to prostrate flowering culms. However, Hilaria, Elymus, Sitanion. Hordeum, however, has there are a few grasses in which cleistogamous a spike with both a single sessile and two short- spikelets are borne on underground culms, e.g. pedicelled spikelets at same node. Amphicarpum purshii, A. muhlenbergianum, and Enteropogon chlorideus. The latter is known com- Whatever the type, inflorescences can be uni- monly as buryseed umbrellagrass because of the form or mixed with separate male, hermaphrodite, spikelet-bearing rhizomes; seed set is highest in female, or sterile spikelets. Tripsacum, for example the cleistogomous spikelets (Barkworth et al. 2003) has proximal spikelets which have female florets (see Chapter 5). only and distal spikelets which have male florets Flowering can occur within 3 months in short- only. Zea mays has separate male and female inflo- lived annuals, or it can be delayed many years rescences (tassels and ears). Bouteloua dactyloides is as in some bamboos. Flowers are borne in sessile dioecious with separate male and female plants. 50 GRASSES AND GRASSLAND ECOLOGY
In this case, differences between male and female may be present, absent, or reduced. The lemma plants of B. dactyloides do not translate into repro- is derived from a leaf sheath and exhibits much ductive allocation, or growth and success in the variation among taxa, making it very important environment (Quinn 1991). taxonomically. The lemma is lanceolate or oval The spikelet is the basic unit of grass systemat- in shape, keeled, texture varying from papery to ics and consists of a shortened stem axis (rachilla) coriaceous, nerved or with 1 to about 15 nerves, plus one to several florets, delimited at the base by firm or hard, dorsally compressed or rounded on two floral bracts, the glumes (Fig. 3.2). The spikelet the back, apices entire (unawned) or bifid with an is a determinate structure, although an exception awn. When present, awns can occur as a projec- to this occurs in the bamboos where psuedospike- tion from the lemma either terminally (ending as lets can occur, e.g. Bambusa and other tropical/ an extension of the midrib) or dorsally (arising subtropical bamboos. A pseudo-spikelet occurs from the back of the midrib). Generally a straight, when glumes subtend a bud which can become a narrow structure, the awn can be bent towards the flowering branch; the flowering branches them- middle, smooth, or setaceous. In Aristida the awn is selves can have glumes subtended by buds which trifid or three-branched. When awned, the lemma can develop. This repeating pattern is iterauctant. base can be reduced to a membraneous bifid scale In a spikelet, one or more florets are grouped or narrow wing. The awn can be hygroscopic together, and usually subtended by two glumes. twisting on being hydrated, allowing the dehisced Glumes are usually membraneous and are bar- grain to move and thus aiding dispersal. Even ren in that there is neither floret or bud in their when not hygroscopic, awns can aid dispersal by axil, and so they are considered equivalent to a enabling the caryopsis to be caught up in animal leaf sheath. Glumes assume a protective function fur or feathers. The palea is a modified prophyll, in the spikelet and can be awned or unawned. usually two-nerved and two-keeled, transparent Spikelets can be perfect, staminate, pistillate, or to glume-like, opposite the lemma, with its dorsal sterile depending upon presence/absence of pistil surface against the rachilla. The palea is without and stamens in the floret (see subfamily character- an awn except in the Australian Amphipogon where istics in Chapter 2). two awns are present on the palea (Bews 1929). Florets (consisting of the lemma, palea, lodi- Grass flowers (lodicule, stamens, and pistil) are cules, stamens, and pistil) are borne on a rachilla hermaphroditic, male or female only, or one or more above the glumes in the spikelet, their number is of each. The floret consists of a pistil with two stig- finite and characteristic of a species, and ranges mas (three in bamboos) and one or two whorls of from 1 per spikelet (e.g. Stipa) to > 40 in Eragrostis three stamens each with an anther attached either oxylepis. Reduction to a single floret per spikelet near the middle (versatile) or at the base (basi- has occurred independently in several groups. fixed) on a slender filament. Exceptionally, there The Pooideae, Chloridoideae, Bambusoideae, and are more anthers, e.g. Ochlandra (Bambusoideae) Arundinoideae mostly have several florets per with 6–120 stamens. The pistil consists of a one- spikelet. The Panicoideae spikelet is two-flowered loculate ovary, with a single ovule, with usually (perfect upper, staminate or sterile lower floret), and two styles and stigmas. The shape of the ovary several pooid and cloridoid grasses have a single varies. Stigmas are two-branched (three-branched perfect floret per spikelet. Florets are either func- in bamboos), feathery, sessile, and elevated on a tional or non-functional. In pooids, non- functional single style or on separate styles. In Zea mays there floret remnants occur furthest away from the is a single long, filamentous style per ovary; the glumes; in panicoids non-functional florets occur ‘silk’ of the corn ear. The ovary, when fertilized, nearest the glumes. produces one seed. There are two membranes at the base of the flo- The lodicules are small narrow scales at the base ret; the palea and the lemma which is below the of the floret. There are normally two inconspicu- palea. The palea, lemma, and floret together form ous lodicules, although some species have one or the anthoecium. Either or both the palea or lemma none, and there are three conspicuous lodicules ECOLOGICAL MORPHOLOGY AND ANATOMY 51 in bamboos. Evolutionarily the lodicules repre- Evolutionary trends in the inflorescence have sent perianth segments. Lodicules are small, pale been the subject of debate for >200 years (Bews green or white and cyclically arranged (like the 1929; Clifford 1986; Kellogg 2001). Condensation stamens, but unlike the alternate glumes, lemmas, (compression and simplification), suppression, and paleas). They become turgid at anthesis, forc- multiplication, and fusion of parts from a relatively ing the floret to open. unspecialized panicle to a derived and reduced The anthers in a grass floret are 1–14 mm in inflorescence with correspondingly reduced spike- length, yellow or cream through pink and red to lets has occurred throughout the family numerous purple, and most are glabrous. Dehiscence is by times (Table 3.1). The evolution of the floret is slits or pores. The pollen varies in size but little in believed to be from a ‘lily’ type ancestor, with morphology, and is more or less spheriodal–ovoid, fusion of carpels (i.e. to a monocarpellate condition) 14–130 μm. There is a solitary ulcerate germination and sharing of a single cauline ovule, reduction of pore surrounded by a distinct annulus, covered stamens from six to three, conversion of three pet- with an operculum. The sexine (outer pollen wall) als (possibly) to three lodicules, and loss to two is either punctate or maculate (i.e. with separate lodicules. The occurrence of petal-identity genes or clustered granules) (Clifford 1986). The limited in the lodicules of maize and rice supports the idea morphological variation of pollen among grasses that the lodicules are reduced, modified petals. The revealed under light microscopy has meant that the three ancestral sepals may have become the palea, presence of grass pollen in palynological samples or the palea and lemma may be derived from asso- generally indicates little more than the presence or ciated floral bracts (Chapman 1996). Other features grasses in the vegetation at the time of deposition. such as the elaboration or loss of awns have been This itself is of value in determining the develop- regarded as evolutionarily advanced (Bews 1929). ment of grassland ecosystems (Chapter 2), but does not allow discrimination among grassland vegeta- 3.7 The grass seed and seedling tion types. development In some genera, glumes, lemmas, or sterile branchlets can become indurated and fused to The fruit of most grasses, known as the caryopsis , form a protective so-called involucre (Bews 1929). consists of a single seed fused with an enclosing For example, in Cenchrus, the involucre consists of pericarp. In common terminology, the grass fruit bristles united at the base to form a spiny cup or or seed is really a seedlike grain consisting of the bur protecting the spikelets. This structure is easily caryopsis either with or without enclosing inflo- caught up in animal skin and fur (causing great pain rescence structures (e.g. bracts, rachilla). The seed in the soles of human feet!), aiding in dispersal. is free from the pericarp in only a few genera,
Table 3.1 Comparison of presumed primitive and advanced grass spikelet characters
Primitive Advanced
Spikelet Large, many-flowered Small, few- or one-flowered Glumes Large, leaflike in texture, several-nerved, Variously modified, reduced or absent, can be awnless or short-awned highly developed for flower protection or seed dispersal Lemma Like the glumes Conspicuously different from glumes Palea Present, two- to many-nerved Nerveless, reduced or absent Lodicules Six or three Two or one Stamens Six, in two whorls Three, two, or one, in one whorl Stigmas Three Two or one
From Gould and Shaw (1983). 52 GRASSES AND GRASSLAND ECOLOGY e.g. Sporobolus, Eleusine, and is then referred to along with seed dormancy and germination cues variously as an achene or utricle. The caryopsis is in Chapter 5. Seed (caryopsis) morphology and either free from the lemma and palea (e.g. wheat) seedling growth is discussed below. or permanently enclosed (Aristida, Stipa, and mem- The grass embryo is highly specialized and bers of Paniceae). In the Andropogoeae, glumes appears as an oval depression on the flat side of the permanently enclose the caryopsis along with a caryopsis next to lemma. On the opposite side of the pedicle and a section of the rachis. The grain may grain to the embryo is the hilum; a line (e.g. Lolium enlarge during development and ripening exceed- perenne, Avena fatua) or dot (Holcus lanatus , Briza ing the size of the glumes, lemma, and palea. In media) marking the point of attachment of the seed some bamboos the pericarp is free from the seed to the pericarp. The embryo includes primordia of and the fruit is a berry that can be as large as one, two, or more foliage leaves and the primary an apple (e.g. Dinochloa, Melocalamus, Melocanna, root, and primordia of several adventitious roots. Ochlandra), or a nut (Dendrocalamus, Schizostachyum, The scutellum is an haustorial organ, equivalent Pseudostachyum) (Bews 1929). to the single cotyledon, and functions in enzyme The caryopsis alone is rarely the unit of disper- secretion and absorption of nutrients from the sal in grasses. Disarticulation of grass diaspores endosperm. Also in the embryo is the coleoptile occurs below, between, or above the glumes and (part of the single cotyledon, an open sheath with at all nodes. Panicoideae disarticulate below the a pore at tip, homologue of first foliage leaf), the glumes, in Paspalum and Panicum the spikelets fall epiblast (an outgrowth of the coleorhiza), and the separately. Spikelets can fall in groups, e.g. chlori- coleorhiza (the first part of the plant to emerge on doid grasses. In Schedonnardus paniculatus and some germination, producing a tuft of anchoring hairs, Eragrostis and Aristida spp., the entire inflorescence protecting the radicle; the primary root emerges breaks off, tumbleweed like. Additional examples through it); all are peculiar to the grass embryo. are provided in Table 3.2. Along with other adapta- The embryonic shoot is known as the plumule, tions such as the presence of awns which can be and the embryonic primary root as the radicle. barbed, retorse, or unarmed, the morphology of The mesocotyl is a vascular trace in the scutellum the grass diaspore has important implications for extending down into the coleorhiza and up into the its dispersal. coleoptile. Endosperm occurs as a large elliptical Following dispersal, the grass caryopsis may structure in the seed formed from the fusion of two or may not be ripe and ready to germinate. The polar nuclei of the embryo sac and a sperm nucleus. ecology of seed dispersal is discussed in detail The endosperm provides nutrition for the embryo
Table 3.2 Diversity of grass diaspores
Dispersal unit Example Features
Whole inflorescence Scrotochloa Inflorescence breaks off as a whole unit Spinifex Plants dioecious. Female inflorescence shed entire, male inflorescence sheds spikelet separately Groups of spikelets Tristachya Triad of three spikelets with fused pedicels shed together Whole spikelet Sorghum The functional (sessile) spikelet shed together with the remnant of the non-functional (pedicellate) spikelet Whole anthoecium Hordeum Palea and lemma adherent to the caryopsis Caryopsis only Triticum Cultivated wheat which is free threshing Seed only Sporobolus (some) Caryopsis modified to extrude a mucilage-coated seed Multiple dehiscence Catalepsis Rachis fragments after which spikelets are then separately deciduous ‘Adherent’ dispersal Aristida (some) A tumbleweed-like ‘grass ball’
From Chapman (1996). ECOLOGICAL MORPHOLOGY AND ANATOMY 53 and developing seedling, and is usually solid and starchy (liquid in some including Koeleria, Trisetum, and all Aveneae). Variation in embryo structure is Third leaf related to the presence or absence of the meso- cotyl, the epiblast, the scutellum cleft (i.e. whether Second leaf or not the scutellum is fused to the coleorhiza), First leaf and whether the first leaf is rolled or folded, and allows an evolutionary sequence of embryo types Coleoptile to be recognized (Renvoize 2002). The bambusoid embryo with the epiblast and scutellum present and a folded first leaf is considered to be the most Cotyledonary node roots primitive type. The absence of a mesocotyl and presence of an epiblast compared with the presence of a mesocotyl and a scutellum cleft is consistent Mesocotyl with the division between the BEP and PACCAD clades, respectively (Chapter 2). Mesocotylar roots
3.7.1 Seedling growth
The first sign of germination is a swelling of the Caryopsis caryopsis as it imbibes water, followed by an enlargement of the coleorhiza and coleoptile, and Transitionary node roots then elongation of the primary root as it pushes through the coleorhiza. Two pairs of transitory node roots develop within a few hours or days (Fig. 3.9). Primary seminal root The primary root and transitory node roots consti- tute the seminal or primary root system, consisting of 1–7 roots, depending upon the species and the environment at the time. Mesocotyl roots can arise Figure 3.9 Hypothetical grass seedling showing development of adventitiously from the mesocotyl. The coleoptile adventitious roots (cotyledonary node roots and mesocotylar roots). is negatively geotropic and positively phototropic, Reproduced with permission with permission from Gould and Shaw and it grows up enclosing the primary shoot and (1983). mesocotyl. The coleorhiza is positively geotropic, and produces the primary seminal roots and tran- sitory node roots. The prophyll emerges first from developmental growth stages. For example, in rice the coleoptile. Emerging from the coleoptile, the (Oryza sativa), seedling, vegetative, and reproduc- primary shoot consists of a culm and several leaf tive stages based on morphological criteria can be stages, and produces cotyledonary node roots recognized (Counce et al. 2000). Seedling develop- (crown roots) which appear at the third leaf stage. ment consists of unimbibed seed (S0), radicle and The mesocotyl and cotyledonary node roots are coleopotile emergence (S1, S2), and prophyll emer- the only roots of mature plants; the seminal roots gence (S4) stages; vegetative development consists remain alive and active as absorbing organs for up of V1, V2 . . . VN stages where N denotes the number to 4 months before dying. In Bromus inermis, for of leaves with collars on the main stem; and repro- example, adventitious roots begin between 5 and ductive development consists of 10 growth stages; 14 days of germination, and by 40 days, adventi- panicle emergence (R0) and development (R1, R2, tious roots constitute 50% of the total roots. R3), anthesis (R4), and grain development (R5–R9). Growth of the grass plant from seedling to inflo- Recognition of developmental growth stages rescence maturity can be expressed in a series of provides a management aid for growers as well 54 GRASSES AND GRASSLAND ECOLOGY as a means of communicating growth data among A number of bundles anastomize at each node researchers. keeping the total number approximately the same throughout. 3.8 Anatomy Bundles vary in size; the central bundle of leaves is the largest, leading to a well-defined Anatomically, the grasses share a number of the midrib in many species. Larger and smaller bun- characteristic features of other monocots, i.e. dles occur in alternating series on either side closed collateral vascular bundles each enclosed of the midrib. Strengthening sclerenchyma is in a sheath of parenchyma, parallel venation in associated with the larger bundles in leaves and the leaves, possession of a single cotyledon, and a stems. general absence of regular secondary thickening (Mabberley 1987). Additional features specific to 3.8.2 Roots the grasses are described below. Adventitious roots arise in parenchymatous ground tissue at the nodes, just below the inter- 3.8.1 Culms calary meristem. The vascular system of a grass Vascular bundles may be scattered through root is a discrete polyarch. Large roots have 10–14 the ground parenchyma of internodes (when exarch xylem groups alternating with groups of solid), or occur as one, two, or more concentric phloem around a central pith. A 1–2-layered pericy- rings. Scattered bundles occur in most tribes, cle is usual, but is not always present. Endodermal concentrically arranged bundles occur in all cell walls thicken as the root matures, caspar- except the Andropogonea and Paniceae. Stems ian strips occur on radial cell walls, parenchyma are generally hollow in pooids and solid in pani- cells occur between the xylem and phloem, and coids. When hollow, vascularization is confined to pericycle and central pith cells lignify as the root the cylinder wall; when solid, it is scattered partly matures. The cortex remains parenchymatous and through the central pith but is most concentrated may break down in older roots. In some species the towards the outside. Strengthening sclerenchyma cortex is interspersed with cavities, e.g. the semi- occurs close to the vascular bundles. In bamboos aquatic Hymenachne amplexicaulis whish has large the whole ground tissue can become lignified, air spaces in the cortex (Renvoize 2002). In small providing immense strength. roots; the vascular tissues form a protostele with a The vascular bundles of stems and leaves pos- single large metaxylem vessel. sess two very large metaxylem vessels outside a row of smaller metaxylem, with protoxylem 3.8.3 Leaves to the inside. The phloem is to the abaxial side of the metaxylem and has clearly differentiated The ground tissue (mesophyll) of a grass leaf con- sieve tubes and companion cells. A cavity occurs sists of short chlorenchyma cells and colourless on the adaxial side of the metaxylem in place of parenchyma cells. Palisade and spongy layers are protoxylem; this cavity is due to differences in rarely differentiated in grasses. The chloroenchyma elongation rates and differentiation of xylem and cells are thin walled and vary from being irregu- cells. In leaves, the vascular strand is enclosed by lar in shape with air spaces to tightly packed with photosynthetic tissue. a moderate to distinctly radiating arrangement Vascular bundles from leaves pass vertically around the vascular bundles. The vascular bundles down the culm, remaining unbranched through are surrounded by a bundle sheath comprising one several internodes before bifurcating and then join- or two cell layers. The outer layer (or single layer ing the vascular bundles of the stem at the nodal when there is only one) is a parenchyma sheath plexus. At this point anastomosis (cross-linking) comprised of thin-walled cells. The inner cell layer of vascular strands occurs, allowing assimilate (the endodermis or mestome sheath) is comprised movement across the plant and between leaves. of small cells with thickened inner and radial Table 3.3 Six types of leaf-blade anatomys
Pooid (festucoid) Bambusoid Arundinoid Panicoid Aristidoid Chloridoid (Aristida only)
Inner mesotome Well developed, Present Poorly defined with Typically lacking, Lacking Present at least around largest sheath/ endodermis thick-walled cells thin cell walls although present bundles in e.g. Eriochloa sericea Outer parenchyma Very indistinct. Small Present, always Large cells lacking Large cells with or Present as double layer, Single cell layer with specialized sheath thin-walled cells, thick-walled and chloroplasts without starch inner sheath cells larger plastids with chloroplasts round/elliptical plastids than outer. Cell walls thick with chloroplasts with specialized plastids Chlorenchyma of Loosely or irregularly Arm-cells with Cells tight or densely Irregular or radiate Long-narrow radially Long, narrow, cells in one layer mesophyll arranged. Large air large fusoids cells packed. Arm-cells from parenchyma arranged cells around radiating from bundles, with spaces. Cells with perpendicular to occasional, fusoid- sheath vascular bundles few chloroplasts chloroplasts. vascular bundles cells lacking. Specialized cells for Lacking Lacking Present in some Present in some Present Present starch storage (Kranz genera genera cells)
After Brown (1958). 56 GRASSES AND GRASSLAND ECOLOGY
(a) walls. Six types of bundle sheath are recognized s st on the basis of the variation in anatomy (Brown 1958) (Table 3.3). These six types correspond to environmental conditions, with the aristidoid and chloridoid types being typical of arid land grasses o possessing the C4 photosynthetic pathway (Chapter 4). The pooid, chloridoid, and arundinoid types are i m illustrated in Fig. 3.10. Sclerenchyma fibres are associated with most vascular bundles, except the smallest, and/or the fibres occur in clusters. The fibres can be continu- ous from the vascular bundle to the epidermis forming a girder or I-beam construction (Gould s and Shaw 1983; Metcalf 1960) (Fig. 3.10c). The cells of leaves that are specialized to carry (b) out malic or aspartic acid decarboxylation and
the Calvin–Benson cycle part of C4 photosyn- thesis (Chapter 4) are known as Kranz cells (Brown 1974, 1975). The term was coined by D.G. Haberlandt in 1882, describing the circular leaf sheath in the Cyperaceae. Kranz is a German word meaning wreath, ring, or rim. Kranz cells occur in 10 families of angiosperms: in monocots in the Poaceae and Cyperaceae, and in dicots in the Amaranthaceae, Chenopodiaceae, Asteraceae, Euphorbiaceae, Molluginaceae, Nyctaginaceae, Portulacaceae, and Zygophyllaceae. Kranz cells are associated with physiological, anatomical, and cytological specialization. These cells are confined usually to the parenchyma sheath surrounding (c) the vascular bundle of leaves. The cells are elon- gated, parallel to the main axis of the bundle. In the grasses, Kranz cells and the associated Kranz anat- omy is restricted to the Panicoideae (some spp.), Chloridoidea (all members), Aristoideae (except Sartidia), and Arundinoideae (Stipagrostis, Aristida, Asthenatherum, Alloeochete) subfamilies.
The mesophyll (m) consists of large, loosely and irregularly arranged chlorenchyma cells. Sclerenchyma strands (s) above and below the vascular bundle forms an ‘I-beam’ girder of supporting tissue. (b) Bouteloua hirsuta var pectinata, chloridoid-type leaf showing large outer bundle sheath and irregular inner sheath of smaller cells with uniformly thickened walls. Small, tightly packed, radially arranged chlorenchyma cells surround the Figure 3.10 Leaf anatomy of grasses. Portions of transverse leaf bundle illustrating typical Kranz anatomy. (c) Cortaderia selloana, sections: (a) Poa sp., pooid-type leaf; note double vascular arundinoid-type showing one large vascular bundle with outer sheath of large, thin-walled outer cells (o) lacking chloroplasts or parenchyma sheath (o) lacking chloroplasts Reproduced with and small inner cells (i) with thickened inner and radial walls. permission from Gould and Shaw (1983). ECOLOGICAL MORPHOLOGY AND ANATOMY 57
The characteristics of Kranz cells in the grasses Kranz Panicoideae has usually one sheath (Kranz include: walls thicker than mosophyll cells and sheath) although a mestome sheath is present in with numerous pits and plasmodesmata; chloro- some taxa. In the Arundinoideae, Stipagrostis of the plasts different from mesophyll chloroplasts (large Aristideae tribe has two sheaths; the outer is Kranz, size, high number per Kranz cell, specific posi- and the inner comprises thin-walled cells without tions within the cell, and many large grana). In chlorophyll and is not considered a mestome, and the Chloridoidea and Aristoideae the Kranz paren- in Aristida there are two chlorophyllous Kranz chyma sheath is exterior to the mestome sheath. sheaths (i.e. a double parenchyma sheath). CHAPTER 4 Physiology
The primary form of food is grass. Grass feeds the ox: the which energy is captured from sunlight, oxygen ox nourishes man: man dies and goes to grass again; and is released from water, and the energy carrier so the tide of life, with everlasting repetition, in continu- molecules of adenosine triphosphate (ATP) and ous circles, moves endlessly on and upward, and in more nicotinamide adenine dinucleotide (NADPH) are senses than one, all flesh is grass. produced are also the same in all grasses regard- John James Ingalls (1872), Kansas, less of whether or not the C4 pathway is present. US Senator 1873–1891 The main differences between C3 and C4 grasses are presented below in this section and summa- Grasses are remarkable in their combination of sev- rized in Table 4.1. eral unique physiological features. These include the possession in more taxa than any other group 4.1.1 Discovery of the C pathway of the advanced C4 photosynthetic pathway (§ 4.1), 4 highly nutritious forage (§ 4.2), the production The C4 pathway was discovered in the economi- of economically important chemicals including cally important sugar cane (Saccharum officinarum) starches, sugars, and other carbohydrates (§ 4.3), and maize (Zea mays) with details of C4 photosyn- and the possession of large amounts of silica in thetic carbon metabolism being described by the their tissue (§ 4.4). All of these physiological fea- Australian physiologists M.D. Hatch and C.R. Slack tures, and others, fundamentally affect the ecology in 1966. Soon after this discovery it was realized of grasses (§ 4.5), and are described in this chapter. that the specialized Kranz anatomy of leaves (Chapter 3) was associated with photosynthesis, that C plants have higher 13C/12C ratios in their tis- 4.1 C3 and C4 photosynthesis 4 sues than C3 plants, and that C3 and C4 plants have More so than any other group of plants the grasses different phytogeographic distributions in relation have evolved an advanced mechanism of CO 2 to climate (Hattersley 1986). assimilation, the C4 dicarboxylic acid pathway. The C pathway, as it is known, allows the plant to con- 4 4.1.2 Distribution and evolution of the centrate atmospheric CO2 in such a manner as to avoid photorespiration. As a consequence, plants C4 pathway in grasses possessing the C pathway have an advantage 4 The C4 pathway occurs in about half of the Poaceae over plants in which this pathway is absent (i.e. C3 (i.e. in c.4500 species). Of the 12 subfamilies plants) in hot and dry environments. The outcome (Chapter 2), the Chloridoideae are predominantly is a fundamental difference in the ecology of C vs 4 C4 with only some C3 members, the Artistidoideae C plants that is manifest at scales ranging from a 3 has both C3 and C4 members, and the Panicoideae few metres to biomes. It is important to remember has taxa representing all the types of C4 pathways that all grasses operate a fully functional C path- 3 along with some C3/C4 intermediates. The other way; the C4 pathway is a supplemental pathway nine subfamilies, including all of the BEP clade, present in some. The light-dependent reactions in are exclusively C3, or in the case of the primitive
58 PHYSIOLOGY 59
Table 4.1 Summary of differences between C3 and C4 grasses. Note: several taxa exhibit intermediate characteristics
Character C3 grasses C4 grasses
Systematics and anatomy Systematic occurrence in grasses All grasses, BEP clade members Most members of Chloridoideae,
exclusively C3 Aristidiodeae, Panicoideae Leaf anatomy No Kranz anatomy Kranz anatomy (bundle sheath cells)
Location of release of CO2 to Calvin cycle Chloroplasts in mesophyll Chloroplasts in bundle sheath cells Physiology
Initial CO2 fixing enzyme RUBP carboxylase/oxygenase (Rubisco) PEP carboxylase
Initial product of CO2 fixation 2 molecules of PGA PEP Susceptible to photorespiration? Yes No Isotopic 13C/12C ratio –22 to –35 –9 to –18
Internal partial pressure (Pi) of CO2 c.25 Pa c.10 Pa in mesophyll (pattern reversed in bundle
sheath cells for C4 plants).
CO2 compensation point 4–5 Pa, increases rapidly with temperature 0–0.5 Pa
Response to increasing atmospheric CO2 Increased photosynthesis and growth Minimal to no response (at least initially)
Photosynthetic response to increasing O2 Negative correlation Unaffected
Photosynthetic response to increasing Decreases as photorespiration increases High rates of net CO2 assimilation temperature with rising temperature maintained at high temperatures
Photosynthetic response to increasing light CO2 assimilation saturates at high light CO2 assimilation saturates at higher
intensity intensity light intensity than C3 plants.
Enzymatic affinity (Km) of Rubisco for CO2 Low High Water use efficiency (WUE) Low High Leaf tissue N concentration 200–260 mmol N m–2 120–180 mmol N m–2 (with 3–6 times less Rubisco) Nitrogen use efficiency (NUE) and Low High photosynthesis per unit of leaf nitrogen (PNUE). Other Forage quality/digestibility/crude Higher Lower protein level Mycorrhizal symbiosis in low P soil Facultative mycotrophs Obligate mycotrophs Ecological advantage Cool, moist environments Hot, dry, high-light environments
Anomochlooideae, Pharoideae, and Puelioideae, spiralis and Hydrilla verticillata) in the monocots, presumed to be so. Genera that include both C3 and 16 dicot families including some members of and C4 members include Alloteropsis, Neurachne, the Amaranthaceae (e.g. Alternanthera, Amaranthus) and Panicum in the Panicoideae and Eragrostis in and the Chenopodiacea (e.g. some Atriplex, Bassia, the Chloridoideae. A few species possess charac- Suaeda) (Sage 2004). teristics intermediate between those of C3 and C4 Evolution of C4 photosynthesis is believed to be species, including the New World Steinchisma decip- polyphyletic with at least 45 independent origins, iens, P. hians, and P. spathellosa, and the Australian and, in grasses, may have evolved up to 11 times
Neurachne minor. C4 photosynthesis also occurs in a (Hattersley 1986; Sage 2004). Atmospheric CO2 few non-grass angiosperm families, including the levels were high in the Cretaceous but declined
Cyperaceae (sedges, e.g. some Cyperus, Scirpus) and in the mid-Tertiary. Atmospheric CO2 concentra- Hydrocharitaceae (frog’s-bit family, e.g. Vallisneria tions lower than they are at present first occurred 60 GRASSES AND GRASSLAND ECOLOGY
during the Oligocene epoch, 23–34 Ma. The CO2- C3 photosynthesis. A full cycle of the Calvin cycle starvation hypothesis suggests that these condi- reduces 6 molecules of CO2, uses energy from 18 tions, along with aridity in tropical areas, provided molecules of ATP and 12 molecules of NADPH the main selective force favouring evolution of produced in the accompanying light-dependent the CO2-concentrating mechanisms and lack of reactions of photosynthesis, and produces 2 mol- photorespiration in C4 species (Cerling et al. 1998; ecules of glyceraldehyde 3-phosphate (G3P) as Osborne and Beerling 2006), although not neces- product. The cycle begins again with the regenera- sarily the spread of C4-dominated grasslands later tion of RuBP. G3P is transported from the chloro- in the mid-Miocene (Chapter 2) (Osborne 2008). plast to the ground substance (cytoplasmic matrix)
Since C4 photosynthesis represents a complex of the cell where it is rapidly converted to glucose mixture of physiological (e.g. the enzyme PEP car- 1-phosphate and fructose 6-phosphate, precursors boxylase) and morphological (e.g. Kranz anatomy, of sucrose. The G3P that remains in the chloroplast
Chapter 3) traits, it is probable that C4-evolution is converted to starch and stored temporarily dur- evolved early in the Paleocene, perhaps as much as ing the day as grains in the stroma. At night the 50 Ma (Apel 1994). Compared with the evolution of starch can be converted to sucrose and exported oxygenic photosynthesis as a whole, C4 photosyn- from the chloroplast. thesis would have appeared during the second half A problem with C3 photosynthesis is that Rubisco of the last hour over the course of a 24 h time frame has a concentration and temperature-dependent
(Apel 1994). Nevertheless, the oldest undisputed affinity for O2 as well as CO2. The solubility of CO2
C4 fossils are panicoid grass leaves with Kranz declines with increasing temperature more so than anatomy from 12.5 Ma. Isotopic carbon ratios from does that of O2. In addition, substrate-saturated
palaeosols (fossil soils) and the teeth of herbivores enzyme activity (Vmax) of Rubisco increases at a faster in East Africa and North America from 14–20 Ma rate with increasing temperature in the presence of are consistent with the presence of C4 plants in O2 than in the presence of CO2, and proceeds at a mid-Miocene landscapes (Sage 2004). Molecular faster rate (Lambers et al. 1998). Whereas carboxyla- clock evidence on the divergence of maize and tion, as described above, produces two molecules sorghum, and maize and Pennisetum (all C4), sug- of PGA, oxygenation when it occurs produces only gests that C4 photosynthesis arose in plants even one PGA and a molecule of the two-carbon com- earlier during the early Miocene, 23–34 Ma. As pound phosphoglycolate (GLL-P). GLL-P is trans- noted in § 2.4.4, the evolution of C4 photosynthesis ported form the chloroplast and after a series of in grasses allowed the later widespread expansion transformations one molecule of GLL-P is used to of C4-dominated grasslands in low latitudes by the produce a molecule of serine, then glycerate, before end of the Miocene, and temperate C4 grasslands regenerating as PGA. In the process a molecule of by 5 Ma (Cerling et al. 1997; Sage 2004). CO2 and one molecule of NH3 are released. This process is referred to as photorespiration because it depends on light and is a respiratory process 4.1.3 Biochemistry of C4 photosynthesis (releasing CO2). Photorespiration therefore reduces
The primary feature of the C4 pathway that distin- the efficiency of the Calvin cycle, causing a decline guishes it from the C3 pathway is the location and in net photosynthesis at high temperatures. manner in which atmospheric CO2 is taken up. In C3 The uptake of CO2 in C4 photosynthesis pro- photosynthesis a molecule of CO2 is taken up and ceeds to attach bicarbonate from CO2 to phosphoe- enters the carbon reduction (PCR or Calvin) cycle nolpyruvate (PEP) through catalysis by the enzyme in the chloroplast. The CO2 is ‘fixed’ (bonded cova- PEP carboxylase, creating oxalacetate (OAA), a lently) to ribulose 1,5-bisphosphate (RuBP) which is four-carbon organic acid. This reaction takes place split to form two molecules of 3-phosphoglycerate in chloroplasts of the leaf mesophyll where CO2 (PGA), a reaction catalysed by the enzyme RuBP is comparatively abundant. PEP carboxylase only carboxylase/oxygenase (Rubisco) in the mesophyll. catalyses the conversion of PEP to four-carbon PGA is a three-carbon molecule, hence the name organic acids and, unlike Rubisco, is unaffected PHYSIOLOGY 61
by O2 levels. The organic acids are transported sheath that has a suberized lamella. PEP is fixed to chloroplasts in specialized bundle sheath cells with CO2 to give four-carbon oxaloacetate, which where the CO2 is released into the normal Calvin is converted to malate and transported to the cycle. This ‘CO2 pump’ enhances CO2 concentra- bundle sheath chloroplasts where it is decarboxy- tion 10–20-fold at the site of Rubisco in the bundle lated by NADP-malate decarboxylase (aka NADP- sheath cells (Apel 1994). malic enzyme) using NADP as co-factor. Carbon
There are three subtypes of the C4 cycle (Fig. 4.1) is returned to the mesophyll as pyruvate. Toxic related to the nature of the organic acid trans- secondary compounds (§ 4.3) are often present in ported to the bundle sheath cell, the enzyme that NADP-ME plants, whereas they tend to be absent in catalyses the decarboxylation step, the anatomy of NAD-ME C4 plants (Ehleringer and Monson 1993). the bundle sheath cells (Chapter 3), and the facility These compounds can act as feeding deterrents to to reduce CO2 leakage from the bundle sheath back insect herbivores. Such protection from herbivory into mesophyll airspaces. In C3 grasses there are may be necessary to protect the ‘exposed’ protein two layers of cells around the vascular bundles, contained within the long and rectangular thin- neither of which is photosynthetic. In C4 plants, walled bundle sheath cells. By contrast, the bundle there is either a double (XyMS+) or single (XyMS–) sheath cells of NAD-ME grasses tend to be short layer of bundle sheath cells reflecting the presence and cubical, hence with a higher surface to volume or absence, respectively, of a second inner layer, the ratio they are more difficult to crush. The bun- mestome sheath, adjacent to metaxylem. The outer dle sheath cells of NAD-ME grasses protect their tangential and radial cell walls of the bundle sheath protein content better than NADP-ME grasses, cells may also be suberized, reducing CO2 leakage obviating the need for toxic secondary compounds. from the bundle sheath back into the mesophyll. Examples of NADP-ME grasses include Saccharum,
The three C4 subtypes are distinguished according Zea, Sorghum, and genera common in moist to to the decarboxylating enzyme: semi-arid habitats of warm regions. Neurachne, Paractaenum, Paraneurachne and Plagiosetum, all ● The PEP-CK (synonyms PCL and PEP) sub- NADP-ME panicoids, have distributions entirely type has Kranz anatomy and is XyMS+ with restricted to arid climates in Australia (Prendergast suberized lamella. The outer bundle sheath et al. 1986). Most grasses species in the Panicoideae layer is photosynthetic with agranal chloroplasts use the NADP-ME subtype. arranged centrifugally (facing towards the out- ● The NAD-ME subtype is XyMS+ with granal side of the vascular bundle). CO2 is incorporated chloroplasts arranged centripetally (i.e. towards in the mesophyll cells first into oxaloacetate then the inner cell wall), which maximizes the diffu- as aspartate before transport to the bundle sheath sion pathway from the site of CO2 release to the cells where it is converted back to oxaloacetate bundle sheath/mesophyll interface. The bundle by cytosolic phosphoenol pyruvate (PEP carbox- sheath cells lack a suberized lamella and so may ykinase). Carbon is returned to the mesophyll leak CO2 more than the other types but have the as PEP or alanine. Examples include Brachiaria, lowest surface area of bundle sheath cells exposed Chloris, Panicum, Spartina, Zoysia, genera character- to mesophyll tissue or intercellular spaces. CO2 is istic of regions with both dry and wet seasons. In incorporated in the mesophyll and transported Australia, Eragrostis species that are PEP-CK-like as aspartate to the bundle sheath cells where it are most frequent in northern high-rainfall tropical is converted in the mitochondria to malate and and humid subcoastal and coastal areas, compared decarboxylated by NAD-malate decarboxylase with NAD-ME-like species that are more frequent with NAD as a co-factor and transported to the –1 in areas where rainfall is <30 cm yr (Prendergast chloroplasts for incorporation into the Calvin et al. 1986). cycle. Mitochondria are particularly abundant in ● The NADP-ME subtype is XyMS– with large the bundle sheath cells of NAD-ME plants com- agranal C3 chloroplasts (suggesting a poorly devel- pared with in the NADP-ME subtype. Carbon is oped photosystem II) in a single-layered bundle regenerated as pyruvate or alanine and returned Mesophyll cell Bundle sheath cell
NADP-ME Chloroplast Chloroplast Starch DHAP ADP Triose P OAA NADP+ NADPH OAA NADPH NADP+ ATP 5 2 3PGA 3PGA RuBP Malate Malate 1 DHAP NADP+ 3 CO2 CO2 ADP Inter- ATP cellular PEP NADPH NADPH space 3PGA + AMP NADP +PPi ATP
PEP Pyruvate Pyruvate 4
Cytosol Cytosol Sucrose
Cytosol PCK Cytosol Chloroplast Aspartate Aspartate Starch 8
8 OAA Inter- RuBP 5 cellular 3PGA space OAA Chloroplast ATP 6 AMP α-keto- 1 CO +PPi ATP glutamate 2 CO2 PEP PEP Pyruvate Glutamate 4 ADP
Pyruvate Alanine PEP 7 Glutamate Alanine Sucrose α-ketoglutarate 7 Pyruvate
NAD-ME Cytosol Mitochondrion 8 OAA NADH Aspartate Aspartate α 9 -keto- Glutamate Malate glutamate 8 10 Inter- Chloroplast NAD cellular AMP space Pyruvate OAA +PPi ATP CO2 PEP Pyruvate 7 1 4 Chloroplast Starch 5 RuBP CO2 Pyruvate PEP Alanine 7 Triose P Glutamate α-ketoglutarate Alanine Cytosol Sucrose
Figure 4.1 Schematic representation of the photosynthetic metabolism of the three C4 subtypes distinguished according to the decarboxylating enzyme. NADP-ME, NADP-requiring malic enzyme; PCK, PEP carboxykinase; NAD-ME, NAD-requiring malic enzyme. Numbers refer to enzymes: (1) PEP carboxylase, (2) NADP-malate dehydrogenase, (3) NADP-malic enzyme (4) pyruvate-Pi-dikinase, (5) Rubisco, (6) PEP carboxykinase, (7) alanine aminotransferase, (8) aspartate amino transferase, (9) NAD-malate dehydrogenase, (10) NAD-malic enzyme. With kind permission of Springer Science and Business Media from Lambers et al. (1998). PHYSIOLOGY 63
to the mesophyll. This subtype is characteristic of than C4 plants (–9 to –18) (Chapman and Peat 1992). 12 13 members of the Chloridoideae including grasses In the atmosphere CO2 predominates, with CO2 of warm regions, especially in dry habitats, and accounting for only 1%. Rubisco reacts more readily 12 13 includes Buchloë, Cynodon, Eragrostis, Panicum, with CO2 than it does with the heavier CO2, so the 13 13 Sporobolus, Triodia, and Triraphis. NAD-ME species enzyme discriminates against CO2. Excess CO2 were found to be most frequent in arid climates in diffuses back to the atmosphere, so plant material Australia (Prendergast 1989). has less 13C than the atmosphere. However, there is less discrimination against 13CO in C plants Ecologically, as described above, there are dif- 2 4 because (1) 13CO that is discriminated against by ferences in the distribution of the three C sub- 2 4 Rubisco in C plants is prevented from escaping types. However, C subtype is not necessarily an 4 4 because of a diffusion barrier between the bundle adaptation to a particular climate and is not the sheath and mesophyll, and (2) excess 13CO is scav- sole determinant of distribution. For example, in 2 enged by PEP carboxylase and carbonic anhydrase Australian Eragrostis species, distribution was more (Lambers et al. 1998). The result is that the 13C/12C closely related to Kranz anatomy cell chloroplast ratio can be used as a ‘signature’ of the relative position than C subtype: species with centrip- 4 contribution of C and C plants in organic matter etal chloroplasts were dominant in arid climates 3 4 such as forage, unidentifiable roots, paleosoils, or whereas more humid climates were dominated by animal tooth enamel (e.g. Cerling et al. 1993). For species with centrifugal/peripheral chloroplasts example, examination of isotope ratios in the diet (Prendergast et al. 1986). of extant elephants (Loxodonta in Africa, Elephas At least 20 plant species, including a number in Asia) indicated a diet dominated by C browse of grasses, exhibit anatomical and biochemical 3 (Cerling et al. 1999). Isotope ratios in soil organic features that are intermediate between C and C 3 4 matter in late Holocene paleosoils indicated the plants. These C /C intermediates have a weakly 3 4 occurrence of C plants, suggesting an early expan- developed Kranz anatomy similar to the NAD-ME 4 sion of tropical high-altitude grassland (páramo) in subtype and Rubisco is present in both the meso- areas of the Bogota basin in the Columbian Andes phyll and the bundle sheath cells. Hence there are that are today dominated by native C vegetation reduced rates of photorespiration and low CO - 3 2 (Mora and Pratt 2002). compensation points compared with C3 plants. Two main types of C3/C4 intermediates are recognized: 4.1.4 Effects of C4 photosynthesis on light, ● C enzyme activity is very low so there is no 4 temperature, and moisture responses functional C4-acid cycle, but these plants possess Biochemical differences between C and C photo- light-dependent recapture of CO2 by the mesophyll 3 4 synthesis lead to a number of profound physiologi- cells following CO2 release in photorespiration in cal differences between grasses possessing these the bundle sheath cells. Thus, CO2 is scavenged, lowering the compensation point. Examples of this two pathways. The most important differences described in detail below relate to the advantage type of C3/C4 intermediate include some species of Neurachne and Panicum. that C4 plants have over C3 plants in warm and arid environments. Briefly, C plants are able to main- ● High activity of C enzymes and CO is rapidly 4 4 2 tain high photosynthetic rates at high temperatures fixed into C4 acids and transferred to the Calvin cycle. However, there is only limited operation of (due to lack of photorespiration) and have high the C cycle, and CO is not effectively concentrated water use efficiency (WUE) (due to low internal 4 2 CO levels, allowing low stomatal conductance for in the bundle sheath cells to allow the low quantum 2 the same CO2 assimilation rates) and nitrogen use yields characteristic of true C4 plants. An example is the Australian grass Neurachne minor. efficiency (NUE) (due to lower requirements for nitrogen-rich Rubisco). C and C plants differ in the 13C/12C ratio in tis- 3 4 The CO2 compensation point (the point at which sues with C plants having lower values (–22 to –35) 3 CO2 uptake equals CO2 evolution) is lower in C4 64 GRASSES AND GRASSLAND ECOLOGY
than in C3 plants (0–0.5 Pa CO2 and 4–5 Pa CO2, high light intensity as CO2 assimilation becomes the respectively). Thus, C4 plants are better able to limiting factor for accumulation. The slope of this fix CO2 when the stomata are closed, and thus to curve is steeper in C4 than in C3 plants, independent conserve water in dry conditions. The CO2 com- of O2 concentration (not the case for C3 plants), and pensation point of C3 plants is sensitive to tempera- saturates at a higher light intensity. Thus, C4 plants ture, increasing rapidly as temperature increases have an advantage over C3 plants in high-light, open
(Williams and Markley 1973). This gives C4 plants environments. an additional physiological advantage over C3 At high temperatures (i.e. <25–30 °C), quantum plants at higher temperatures. C4 photosynthesis is yield and light-use efficiency (LUE) of C3 plants also unaffected by O2 concentration (because of the is low, and declines with increasing temperature lack of photorespiration), whereas C3 photosynthe- as the oxygenating activity of Rubisco increases sis declines as oxygen concentration increases. (i.e. as photorespiration increases). By contrast, the
The internal partial pressure (Pi) of CO2 in the quantum yield of C4 plants is high and unaffected mesophyll is c.25 Pa in C3 plants compared with c.10 by temperature. At low temperatures, the quantum
Pa in C4 plants; however, this pattern is reversed yield and LUE of C4 plants is lower than that of in the bundle sheath cells where CO2 is released C3 plants because C4 plants require two additional to the Calvin cycle in an environment that is not ATP molecules derived from the light-dependent compromised by photorespiration. High Pi of CO2 reactions to regenerate one molecule of PEP from in the bundle sheath allows for favourable kinetic pyruvate. This gives C3 plants an advantage over properties of Rubisco in the bundle sheath to be C4 plants at low temperatures. Hence, because taken advantage of. In C4 plants the enzymatic dis- of the lack of photorespiration in C4 plants, LUE sociation constant (the Michaelis–Menten constant, is unaffected by temperature whereas it declines
Km (CO2)) for Rubisco is high (i.e. the enzyme has a with temperature in C3 plants. low affinity for its substrate), meaning that CO2 is Tissue nitrogen levels are lower in C4 plants –2 not as tightly bound to Rubisco as is necessary for (120–180 mmol N m in leaves) than in C3 plants –2 C3 plants. High Km for Rubisco in C4 plants allows (200–260 mmol N ) (Ehleringer and Monson 1993) for a high (fast) catalytic activity leading to more because 3–6 times less of the nitrogen-rich Rubisco moles of CO2 to be fixed per unit of Rubisco and is needed and because of the low levels of photores- time compared with C3 plants. In addition, the Km piration enzymes. Consequently, NUE and PNUE for CO2 of PEP carboxylase is lower (hence, high (photosynthesis per unit of leaf nitrogen) is high in affinity) than the Km for Rubisco in C4 plants. C4 plants. However, high PNUE does not appear to
The WUE is high in C4 plants because stomata translate into an advantage for C4 plants on low- of C4 plants need not be opened and subject to nitrogen soils (Lambers et al. 1998). transpirational water loss for as long or as exten- sively as those of C species to assimilate CO at 3 2 4.1.5 Ecological ramifications a given rate. C4 plants can produce 1 g of biomass per 250–350 g of water transpired, whereas C3 Tropical areas where C4 photosynthesis evolved plants transpire 650–800 g water for every gram of continue to be centres of distribution for C4 plants biomass produced (Ehleringer and Monson 1993). including grasses. C4 species dominate tropical
Consequently C4 plants may be advantaged in arid and temperate grasslands with abundant warm- environments. For example, WUE was 40–170% season precipitation. The frequency of C4 grasses greater for the C4 grass Andropogon gerardii than for correlates positively with minimum growing sea- co-occurring C3 forbs, although during a wet year son temperatures (Terri and Stowe 1976). For exam- there were no differences in maximum rates of ple, the geographic distribution of C4 grass taxa photosynthesis between the two groups of plants in North America ranges from 12% of the grass (Turner et al. 1995). taxa in the north to 82% in the desert south-west Light response curves (plots of photosynthetic rate (Fig. 4.2). Along the Atlantic and Pacific coastal vs light intensity) for C3 plants saturate (i.e. flatten) at regions, the proportion of C4 grasses increases as PHYSIOLOGY 65
6 genera) and was intermediate between the other 2 subtypes in its distribution, although PEP-CK grasses were also somewhat confined to rock crev- ices and irrigated fields. At more local scales, numerous studies docu- 12 12 ment differential distribution of C3 and C4 grasses in response to local moisture, irradiance, and 13 31 22 23 12 34 temperature gradients (e.g. Archer 1984; Barnes 18 38 37 34 26 40 35 et al. 1983; Gibson and Hulbert 1987). For example, 50 46 18 52 48 in the Mule Mountains of south-east Arizona, USA, 57 61 37 82 54 69 C species representing 6 angiosperm families 68 4 80 were encountered accounting for 13.5–22.3% of vas- cular species (69–96% of the Poaceae encountered) in vegetation ranging from pygmy conifer-oak scrub (Pinus cembroides, Junierus deppeana, Quercus 0 500 1000 km arizonica, Q. hypoleucoides, and Q. emoryi) in mesic areas to desert grassland (Elyonurus barbiculmis, Bouteloua radicosa, Heteropogon contortus) in xeric Figure 4.2 Geographic distribution of C4 grass taxa in North America. Numbers indicate the percentage of grass taxa that are situations (Wentworth 1983). The proportion and C . With kind permission of Springer Science and Business Media 4 percentage canopy cover of C4 species increased from Lambers et al. (1998), redrawn from Terri and Stowe (1976). with increasingly warm and dry environmental conditions in vegetation occurring over granite. latitude decreases on both coasts and as July mini- In contrast, vegetation occurring over limestone mum temperature increases (Wan and Sage 2001). that had been heavily grazed did not show this
The proportion of NADP-malic enzyme C4 grasses relationship. was positively correlated with mean annual Even on a small spatial scale, local soil moisture precipitation. conditions can lead to differences in the abundance
Along a north–south gradient from North of C3 vs C4 taxa in grasslands. For example, across
Dakota to south Texas the C3/C4 ratio of graminoids a 400 m hillside in remnant mixed-grass prairie decreased from 1.9 to 0.8 in a survey of remnant true in Colorado, USA, three C4 grasses (Bouteloua gra- prairie in North America, and was negatively cor- cilis, B. curtipendula, and Schizachyrium scoparium) related with annual precipitation and temperature, were found to dominate the rocky, dry mid-slope, and positively correlated with soil organic matter whereas C3 grasses dominated the moister top (Diamond and Smeins 1988, and see § 6.1.2). In the (Pascopyrum smithii) and bottom (Poa pratensis) Sinai, Negev, and Judean deserts of the Middle (Archer 1984; Barnes et al. 1983).
East, the occurrence of C4 grasses increased with Overall, it remains unclear whether it is temper- decreasing rainfall (Vogel et al. 1986). C4 grasses ature or moisture that determines the differential were found to dominate areas of high year-round distribution of C3 and C4 grasses. More than likely temperature. The NADP-ME C4 subtype (27 species it is the interplay between these two factors that is in 18 genera) was most frequent where water stress important (Vogel et al. 1986). was not a dominating factor (such as in rocky crev- ices and irrigated fields) whereas the NAD-ME 4.1.6 Effects of global climate change subtype (16 species in 7 genera) was most frequent in xeric, open desert areas. NADP-ME grasses Global temperature and atmospheric CO2 levels were mostly summer active perennials, whereas have been increasing due to anthropogenic the NAD-ME subtype was represented mostly by causes for the last 250 years, since the start of the winter perennials. The PEP-CK subtype was not Industrial Revolution. The Intergovernmental abundant in this Middle Eastern flora (10 species in Panel on Climate Change predicts that atmospheric 66 GRASSES AND GRASSLAND ECOLOGY
CO2 will double in the mid–late twenty-first cen- grass Andropogon gerardii in a North American tall- tury and cause a 1.4–5.8 °C rise in mean temper- grass prairie, reductions in photosynthesis related ature (IPCC 2007). Because CO2 is a substrate for to water stress were less likely to occur under
photosynthesis, increased atmospheric CO2 may elevated than ambient CO2 levels (Knapp et al. 1993; substantially increase photosynthetic rates and Nie et al. 1992a). growth, decrease leaf transpiration through sto- The differential response of C3 and C4 plants to matal closure, and increase WUE of land plants. elevated CO2, coupled with a predicted increase
For C3 plants in particular, increased atmos- in global temperature, has the potential to affect pheric CO2 provides a large ‘fertilization’ effect competitive interactions among plants, alter com- by decreasing photorespiration and increasing munity composition, and elevate grassland eco- carbon assimilation rates. Experimental studies of system production by about 17% (Campbell and
C3 grasses conducted at elevated (mostly double Stafford Smith 2000; Navas 1998; Polley et al. ambient) CO2 levels (i.e. c.760 µg g CO2) generally 1996; Soussana and Luscher 2007). When grown show an c.34–44% increase in growth (Amthor in competition, C4 species show lower responses
1995; Kirschbaum 1994; Long et al. 2004; Poorter to elevated CO2 at high nutrient conditions than
1993). However, the increased photosynthetic do C3 grasses or dicots (Poorter and Navas 2003). rates may be short-lived as some plants grown Given that C4 plants may be less negatively affected under elevated CO2 in open-top chambers accli- by higher temperatures than C3 plants, the overall mate or down-regulate producing less Rubisco, effect of elevated CO2 coupled with rising global lowering carbon allocation to leaves, decreasing temperature is difficult to predict, especially leaf stomatal density, or decreasing expression of since elevated CO2 can vary with abiotic factors specific photosynthetic genes or gene products (Soussana and Luscher 2007) and affects rates of in response to increased sucrose cycling within decomposition and soil nutrient mineralization mesophyll cells (Long et al. 2004). A meta-analysis in complex ways. There clearly are limits on how of published studies suggests that this effect rep- reliably we can predict vegetation patterns from resents more of an acclimation of the plant to the leaf physiology. Several experimental studies have changed conditions (such as constrained rooting observed effects of elevated CO2 on grassland volume or nutrient limitation) rather than a down- communities in which the proportion of grasses regulation per se of gas exchange to former levels to forbs has declined (e.g. Potvin and Vasseur
(Long et al. 2004). Plants grown under elevated CO2 1997; Teyssonneyre et al. 2002; Zavaleta et al. 2003). in field settings (so-called free-air CO2 enrichment Winkler and Herbst (2004) observed a shift in or FACE experiments) show declines in Rubisco botanical composition reflecting an increase in accompanying increased photosynthetic rates, but legumes in a nutrient-poor, calcareous semi-natu- no change in capacity for ribulose-1,5-bisphosphate ral grassland (Bromus erectus dominated) subjected regeneration. High growth rates under elevated to 4 years of elevated CO2.
CO2 without increased availability of soil nitrogen Global circulation models (GCMs) project some- can lead to lowered tissue nitrogen levels (‘nitro- times significant changes in abundances of C3 and gen dilution’) and altered protein composition C4 plants under various climate change scenarios (Newman et al. 2003). that include elevated temperature and higher
By contrast, C4 plants, including C4 grasses, are atmospheric CO2. For example, Epstein et al. (2002b) not limited by CO2 levels and so exhibit smaller projected an increase in the relative abundance of growth responses than C3 plants to elevated atmos- C4 grasses by >10% throughout most of the temper- pheric CO2 levels in the range of 10–25% (Long et al. ate grasslands and shrublands of North and South
2004; Wand et al. 1999). Positive growth responses America at the expense of C3 grasses (Fig. 4.3). These of C4 grasses to elevated CO2 often are due to projections are consistent with predictions under
CO2-induced stomatal closure and enhanced water higher temperatures but do not match with the sug- use efficiency rather than to a direct enhancement gestion that C3 species will benefit at the expense of photosynthetic rates. For example, in the C4 of C4 species under elevated CO2. Indeed, some PHYSIOLOGY 67
GFDL GISS
Change of C4 Grass Decrease > 20% Decrease > 10–20% No change Increase 10–20% Increase > 20%
UKMO
Figure 4.3 Projected absolute percentage change in C4 grass abundance for double CO2 scenarios in three general circulation models (GFDL, GISS, and UKMO). Reproduced with permission from Epstein et al. (2002b).
field studies have shown no competitive advantage atmospheric CO2 and other aspects of the climate, of C3 over C4 grasses under high CO2 (Owensby et such as temperature and precipitation, that are pre- al. 1993). The benefit of elevated CO2 for C3 plants dicted to be affected under global environmental appears to be contingent on temperature and mois- change (Norby and Lou 2004). For example, pho- ture; if it is too hot and too dry then C4 plants main- tosynthetic pathway and precipitation were iden- tain their competitive advantage even with elevated tified as the most important variables affecting
CO2 (Nie et al. 1992b). The importance of multifactor foliage production in a modelling study of semi- experiments is clear given the interactions between humid temperate grassland subjected to various 68 GRASSES AND GRASSLAND ECOLOGY climate change scenarios that included increased is measured by feeding animals and weighing growing season precipitation and temperature fecal dry matter output. In vitro digestibility (in while maintaining current atmospheric CO2 levels vitro dry matter disappearance: IVDMD) involves (Seastedt et al. 1994). the inoculation of forage in rumen fluid to simulate the ruminant digestive tract. Digestibility is not 4.2 Forage quality usually measured by commercial forage-testing laboratories. Forage is defined as any plant material, including Relative feed value (RFV) (Collins and Fritz herbage but excluding concentrates, used as feed 2003) provides a single value for comparing forages for domestic herbivores (see Table 1.2). This techni- and is based on the negative correlation between cal definition is somewhat narrow, and for an eco- ADF and digestibility and between NDF and vol- logical perspective forage should include the plant untary intake (quality of forage that animals con- material in grasslands that is feed for native her- sume given an unrestricted supply). Thus, bivores (Chapter 9). Forage quality is the potential RFV (DDM DMI)/1.29 of a forage to produce the desired animal response, with forage nutritive value as the nutrient concen- where DDM is dry matter digestibility (%) and DMI trations, digestibility (energy value), and nature of is voluntary dry matter intake calculated as: the end products of digestion (by a grazer) (Collins DDM 88.9 (0.779 ADF) and Fritz 2003). The important components of for- age include minerals (nutrient elements), cell-wall DMI 120/NDF carbohydrates (structural carbohydrates), lignin, Near-infrared reflectance spectroscopy (NIRS) crude protein, and non-structural carbohydrates is a non-destructive technique that allows 90–99% (including organic acids, starch, and sugars), pro- accurate estimations of CP, NDF, ADF, and IVDMD teins, and lipids. There is an important feedback with lower costs than the standard wet lab between forage quality and grazer behaviour (see procedures. Chapters 9 and 10). Forage quality is determined ultimately by measuring animal response, such as milk produc- 4.2.1 Differences among species in tion or weight gain, but such feeding trials are forage quality expensive and require extensive labour, animals, and facilities. Laboratory analyses of forage pro- There are important differences among spe- vide information about potential animal response. cies in forage quality, with legumes generally A typical forage analysis report will include values having higher quality than grasses. Legumes for neutral detergent fibre (NDF), acid detergent and cool-season grasses often have similar ADFV fibre (ADF), crude protein (CP), moisture, and min- concentrations and digestibility, but cool-season eral concentration (especially calcium, phosphorus, grasses generally have higher NDF. In a compari- magnesium, potassium, and sometimes sulfur). son between Medicago sativa (alfalfa) and Phleum NDF is the total fibre or cell wall fraction of the for- pratense (timothy), NDF values were 49% and 66%, age following extraction with a neutral detergent respectively and CP values were 16% and 9.5%, solution. ADF is an extract made using 1 N sulfuric respectively (Collins and Fritz 2003). Forage of acid and is made up of cellulose, lignin, and silica. warm-season C4 grasses is of lower quality and Hemicellulose is not extracted with ADF but is esti- c.13% lower in digestibility than that of cool-season mated by subtracting ADF from NDF. C3 grasses because a high percentage of leaf area Digestibility is the proportion of dry matter or is occupied by highly lignified and less digestible constituent digested within the digestive tract of tissues (vascular bundle, epidermis, sclerenchyma) the animal (Barnes et al. 2003) and can be deter- (Fig. 4.4). Crude protein levels in leaves of warm- mined either in vivo or in vitro. In vivo digestibility season grasses are also lower than in leaves of PHYSIOLOGY 69
80 Dairy cow, 57 lb milk/day perennial grasses Legumes annual grasses
Cool season 500 lb steer, Cool season 70 2.5 lb daily gain Tropical annual Tropical perennial grasses
60 grasses Mature brood cow, average milking ability
DM digestibility (%) 50 Dry, beef brood cow (2nd trimester)
40
Major types of forage species
Figure 4.4 Digestibility ranges of major forage types. Dashed lines show forage digestibility levels required to meet energy requirements of different classes of cattle. Reproduced with permission from Collins and Fritz (2003).
90 cool-season grasses. It has been suggested that C3 (4) and C4 grasses may become nutritionally equiva- lent under elevated CO2 because of the generally larger response of C3 species to elevated atmos- pheric CO2. However, this hypothesis was not sup- 80 ported in a comparison of five C3 and C4 grasses grown under elevated CO (Barbehenn et al. 2004); 2 (34) protein levels decreased in the C3 grasses but not to the level of C4 grasses. 70 Forage quality decreases with plant age/ maturity, principally because of a decrease in the leaf:stem ratio (Nelson and Moser 1994). For example, the leaf percentage of total DM declined from 61% to 23% Herbage dry matter digested (%) 60 in Dactylis glomerata from early vegetative stage (40) to late anthesis (Buxton et al. 1987). Leaves repre- sent the highest-quality part of the forage, and are preferentially chosen by grazers when allowed the 50 Ear emergence choice. The proportion of stems increases as the plant matures through the season and stem and (50) leaf quality declines (Fig. 4.5). In Dactylis glomerata May 1 June 1 July 1 the leaf fraction fell more slowly than that of the Whole plant Leaf blade leaf sheath and stem fractions. Leaf sheath Stem Although plant maturity impacts forage qual- Figure 4.5 Decline in forage quality of S. 37 Dactylis glomerata ity more than anything else, maturity is modified in various plant parts during first growth in the spring. Figures by plant environment. Solar radiation is the driv- in parentheses are the percentage of stem in the whole plant. ing force setting an upper limit for production, Reproduced with permission from Bransby (1981). 70 GRASSES AND GRASSLAND ECOLOGY modulated by temperature and rainfall. Light amounts: iron (Fe), chlorine (Cl), manganese (Mn), intensity and quality affect growth processes, i.e. zinc (Zn), molybdenum (Mo), boron (B), and nickel morphogenesis, giving the plant form and affect- (Ni). In addition, sodium (Na) and cobalt (Co) are ing tillering, branching, internode expansion, essential to some plants and are regarded as micro- leaf expansion, and flowering (Nelson and Moser nutrients by some authorities (Whitehead 2000). 1994). The influence of environmental factors on Apart from carbon, hydrogen, and oxygen, which forage quality was illustrated in a comparison of can be taken up through gas exchange via the sto- total non-structural carbohydrate (TNC) levels in mata, the essential elements are taken in through leaves of 128 C3 and 57 C4 grasses grown under root uptake from the soil solution. Metals generally cool (10/5 °C light/dark) and warm temperatures occur as positively charged cations adsorbed to soil (25/15 °C), respectively (Chatterton et al. 1989). The particles, e.g. Ca2+, K+, and Na+, whereas non-metals
C3 grasses accumulated higher TNC levels under occur in the soil solution as negatively charged ani- –1 – 2– both cool and warm temperatures (312 mg kg , ons, e.g. nitrate (NO3 ), sulfate (SO4 ), bicarbonate –1 3– 107 mg kg , respectively) than did the C4 grasses (HCO ), and can be readily leached from there. In (166 mg kg–1, 92 mg kg–1, respectively), mainly due some soils phosphate forms insoluble precipitates to accumulation of fructan in the leaves, especially and is adsorbed and held on the surface of com- in cool conditions. Generally, forage is more digest- pounds containing iron, aluminium, and calcium ible at low temperatures because (1) lignification of so that it is retained against leaching and somewhat cell wall materials increases at high temperatures difficult for plant roots to obtain. Because of this, and (2) accumulation of digestible storage products mycorrhizae are especially important to plants in is greater at low than high temperatures. the uptake of phosphorus as their mycelia increase the surface area available for uptake in the soil compared with non-mycorrhizal roots (Chapter 4.2.2 Nutrient elements 5). C4 grasses are obligate mycotrophs especially Knowledge of nutrient levels in grasses and asso- dependent on soil mycorrhizae for soil phosphorus ciated grassland plants is important in grassland acquisition in low-phosphorus soils (Anderson et agriculture. Bioavailability of nutrients in forage al. 1994; Hetrick et al. 1986). affects grazer diets and nutrition. Much agricul- The concentration of nutrients in the soil of tural research is devoted to improving the mineral natural and semi-natural grasslands normally nutritional quality of forage (Spears 1994). reflects the underlying soil parent material, modi- In addition to carbon (C), hydrogen (H), and oxy- fied by the long-term effects of the environment gen (O), plants require 14 other inorganic elements, and climate (Chapter 7). In these soils, recycling, the nutrient (or mineral) elements. These nutrient including the death and decay of plants, drives elements are referred to as essential elements if: nutrient recycling and plant nutrient uptake. (1) a deficiency makes it impossible for the plant to By contrast, the soils of managed grasslands are complete the vegetative or reproductive stage of its usually supplemented with nitrogen, phospho- life cycle; (2) the deficiency is specific to the element rus, and/or potassium fertilizer, and sometimes in question and can be prevented or corrected only micronutrients, to supplement deficiencies and by supplying this element; and (3) the element is replace loss through the removal of plant and ani- directly involved in the nutrition of the plant and is mal products. Animal excreta are an important not simply correcting some unfavourable condition part of the recycling process in grazed grasslands of the soil or culture medium (Whitehead 2000). (Chapter 9). Legumes are important and significant Macronutrients are those nine essential elements components of temperate semi-natural grasslands, required in large amounts and, in addition to and can fix up to 500 kg N ha–1 yr–1 (Whitehead carbon, hydrogen, and oxygen, include nitrogen 2000). White clover Trifolium repens is the most (N), potassium (K), calcium (Ca), phosphorus (P), important legume in European and New Zealand magnesium (Mg), and sulfur (S). A further eight grasslands, lucerne (alfalfa Medicago sativa), red micronutrients are required in very small, or trace, clover Trifolium pretense, and birdsfoot trefoil Lotus PHYSIOLOGY 71 corniculatus in North America, and annual clovers factors. There is wide variation between nutrient and medics Medicago spp. in temperate areas elements (Table 4.2). Nitrogen exhibits the greatest with a pronounced dry season, including parts of amount of accumulation (10:1), followed by chlorine Australia. (7:1); both are readily taken up from soil solution as –1 + – Acquisition of nutrients occurs principally NO3 or NH4 , and Cl , respectively. Iron shows 5–50 mm back from the root tip. In this region, the greatest degree of exclusion (0.4:1). With the root hairs (protrusions of individual epidermal exception of chlorine, which is involved in water cells c.10 µm in diameter and 0.2–1 mm in length) relations, photosynthesis, and ion homeostasis, the grow into micropores within soil aggregates. Root micronutrients have lower levels of accumulation hairs increase the effective surface absorption area than macronutrients. of the root. An abundance of root hairs and fine roots provides the most effective nutrient uptake Tissue nutrient levels in limited soils. Nutrient ions close to root hairs The levels of nutrients in plant tissues range from move by mass flow or diffusion. The root hairs of 1.0–5.3% for nitrogen to close to zero for elements grasses are longer and more numerous than those such as sodium and molybdenum (Table 4.2). of legumes. Nitrogen is the soil-derived essential element with the highest plant tissue level because of its ubiqui- Plant:soil concentration ratios tous importance in amino acids, proteins, nucle- Differences between elements with respect to otides, nucleic acids, chlorophylls, and coenzymes. accumulation in grassland plants are based on the In particular, Rubisco is the most expensive and nature of the soil and interacting environmental abundant nitrogen compound in plant tissues.
Table 4.2 Typical nutrient levels in grass tissues, adequate tissue levels (concentrations necessary to maintain vital functions) and critical concentrations (concentration in leaves below which reductions in maximum yield of 10% or more may be expected).
Typical Typical concentration Adequate tissue Critical Plant:soil concentration in in herbage dry matter: levels (Taiz and concentrations concentration soil dry matter mean and range Zeiger 2002) (Whitehead 2000) ratio (x:1)
Macronutrients (%) N 0.3 2.8 (1.0–5.3) 1.5 2.5–3.2 10.0 P 0.2 0.4 (0.05–0.98) 0.2 0.12–0.46 2.0 S 0.1 0.35 (0.04–0.43) 0.1 0.16–0.25 3.5 K 1.5 2.5 (0.21–4.93) 1.0 1.2–2.5 1.7 Na 0.3 0.25 (0.00–0.39) 10 – 1.0 Ca 1.8 0.6 (0.03–2.73) 0.5 0.1–0.3 0.33 Mg 0.8 0.2 (0.03–0.79) 0.2 0.06–0.13 0.25 Micronutrients (mg kg–1) Fe 35 000 150 (10–2600) – <50 0.3 Mn 1 600 165 (6–1200) 50 20 0.1 Zn 150 37 (3–300) 20 10–14 0.25 Cu 30 9 (0.4–214) 6 4 0.3 Cl 500 3500 (500–10 000)a 100 150–300 7.0 B505 (1–94)20<60.1 Mo 2.6 0.9 (<0.02–17) 0.1 <0.1–0.15 0.35
Plant:soil levels and concentration ratios of nutrient elements for temperate grasslands from Whitehead (2000) Tables 3.4 and 3.6, based on >12 400 samples from temperate grasslands in Finland, Pennsylvania and New York (USA), and England and Wales. a Source for Cl range: Barker and Collins (2003). 72 GRASSES AND GRASSLAND ECOLOGY
There is a wide range of tissue concentrations for concentrations of tissue potassium have been each element depending upon the stage of matu- reported as 1.6–2.5% for cool-season grasses and rity of the plant, species differences, seasonal and 1.2–2.0% for warm-season grasses depending on weather factors, soil type, and the application of season and cultivar (Cherney et al. 1998). Critical fertilizers (Whitehead 2000). Plant maturity is con- concentrations for sulfur for young grass is 0.16– sidered to be the single factor with the greatest 0.25% (Whitehead 2000). Grasses are rarely defi- impact on forage quality, with the biotic and abiotic cient in calcium or magnesium, but reported critical factors of the environment acting as an important concentrations for Lolium perenne are 0.1–0.3% for modifier (Baxter and Fales 1994). calcium and 0.06–0.13% for magnesium, with the Adequate or minimal levels of the essential variation reflecting plant age. Management affects elements in plant tissues are well known (Table 4.2). critical concentrations of nutrients as grass har- These concentrations are necessary to maintain vested frequently (e.g. through mowing or haying) vital functions. The concentrations required for or grazed may require higher levels of nutrients to optimum growth, stand longevity, and drought maintain high yield levels. resistance varies among species. The critical con- Species differences in leaf tissue content are illus- centration refers to the concentration in the leaves trated for four temperate grasses and the legume red below which reductions in maximum yield of 10% clover Trifolium repens in Table 4.3. Nutrient element or more may be expected as a result of inadequate content was broadly similar among these temper- supply of the nutrient element. Much of what we ate C3 grass species, with no one species having a know about critical concentrations in grassland higher overall level of any one nutrient than the oth- plants is from agricultural work on the principal ers. The plants in this study were grown as mono- species in seeded or semi-natural temperate pas- cultures in field plots treated with NPK fertilizer tures, especially Lolium perenne. Critical concentra- (Fleming 1963). Tissue nutrient content exceeded tions for grasses are reasonably well established minimal levels for most nutrients, but does suggest for the macronutrients, especially nitrogen, phos- possible deficiency for some of the micronutrients, phorus, and potassium, and are discussed below, most notably boron for all the grasses. Similarity in except for sodium which is not reported (Table 4.2). tissue nutrient levels among co-occurring grasses Critical concentrations for the micronutrients are is not always the case, and Cherney et al. (1998) less well known, but are discussed in Whitehead report generally lower levels of tissue potassium in
(2000). Knowledge of critical concentrations is used C4 compared with C3 grasses (1.2–3.8% vs 1.4–5.2%, for making fertilizer recommendations in man- respectively) because of the low soil potassium in aged pastures and for crops. For example, critical many tropical regions. Co-occurring forbs have concentrations for Lolium perenne were established been reported to have higher tissue concentra- as nitrogen 3.2%, potassium 2.8%, phosphorus tions of some nutrient elements than grasses, but 0.21%, sulfur 0.18%, and magnesium 0.07% (Smith this varies depending on the particular mixture of et al. 1985). Tissue nitrogen levels range from 1.0 to the sward. As expected for a nitrogen-fixing leg- 5.3% (Table 4.2) with actual concentration depend- ume, Trifolium repens in Fleming’s (1963) study had ing upon soil supply, species, and stage of maturity almost double the leaf tissue of nitrogen compared of the plant. The critical concentration for tissue with the grasses (Table 4.3). nitrogen depends principally on stage of maturity. Varietal or ecotypic differences may significantly For example, with a 4-week regrowth, critical nitro- affect tissue nutrient concentration, and attempts gen concentration in Lolium perenne was 3.2–3.5%, have been made to breed cultivars with increased whereas with a 6-week old regrowth it was only concentrations of specific nutrient elements. For 2.5% (Whitehead 2000). Critical concentrations of example, genetic variation for 8 of 17 essential tissue phosphorus vary from 0.12 to 0.46% in sub- elements and selectable heritability for tissue tropical and tropical grasses, from 0.20 to 0.34% magnesium, sodium, and phosphorus, but not for in cool-season grasses and from 0.22 to 0.30% in potassium was demonstrated for a Lolium perenne warm-season grasses (Mathews et al. 1998). Critical breeding pool (Easton et al. 1997). In a comparison of PHYSIOLOGY 73
Table 4.3 Nutrient element concentration in leaf tissue (mean of three samples) of four temperate pasture grasses and red clover Trifolium pretense
Nutrient Lolium Dactylis Phleum Schedonorus Trifolium perenne glomerata pretense pratensis pratense
N (%) 2.1 2.8 2.5 2.6 4.2 P (%) 0.32 0.32 0.13 0.3 0.3 K (%) 2.3 2.6 1.7 2.1 1.7 Ca (%) 0.87 0.57 0.88 0.87 2.1 Mg (%) 0.17 0.15 0.27 0.18 0.3 Fe (mg kg–1)1016742109134 Mn (mg kg–1)411053829136 Zn (mg kg–1)2023191642 Cu (mg kg–1)5.07.14.64.917 B (mg kg–1) 9 10 17 10 26 Mo (mg kg–1) 0.47 0.77 0.58 0.60 0.3
From Fleming (1963).
half-sib families of L. perenne in southern Australia, directly involved in the primary catabolic or bio- significant family variance for yield, magnesium, synthetic pathways but play an important role in calcium, and potassium, and family by location the ecological relationship of grasses with their interactions were observed for potassium and mag- biotic environment (Fig. 4.6). Many of these com- nesium indicating genotype × environment effects pounds are toxicants that affect the digestibility on tissue mineral levels (Smith et al. 1999a). and nutritive value of grasses in forage, or affect Tissue mineral concentrations vary considerably herbivore physiology resulting in animal toxicity among plant parts, both seasonally and depending or stress. Other chemicals, and some of the same on stage of maturity. Generally, nutrient concen- ones, are important allelochemicals involved in the trations are highest in young compared with older stimulation or inhibition of neighbouring plants tissues, although the pattern of changes with age (see review by Sánchez-Moreiras et al. 2004). can be erratic for the micronutrients. Nitrogen can The chemical compounds present in non-grass show a 70% reduction in concentration from early components of forage are not discussed here, except spring to midsummer, and phosphorus and sulfur to note that many non-grasses produce toxins that concentrations can decline by 40–60%. Senescing negatively affect forage quality, e.g. plant oestrogens leaves lose nutrients, especially nitrogen, phospho- in subterranean clover Trifolium subterraneum; tan- – rus, sulfur, and potassium, through remobilization nins in legumes; NO3 in the Amaranthaceae (pig- and/or leaching by rain. Calcium and micronutri- weed), Chenopodiaceae (goosefoot), Brassicaceae ent cations show less of a decline, or even a rela- (mustard), Asteraceae (sunflower), and Solanaceae tive increase in concentration in senescing leaves, (nightshade) families; and cyanogenic glycosides in than the other macronutrients as they are relatively Prunus virginiana and Pteridium aquilinum (Nelson immobile (Whitehead 2000). and Moser 1994). The secondary compounds of ecological impor- 4.3 Secondary compounds: tance in grasses are considered below under four anti-herbivore defences and major classes; nitrogen compounds, terpenoids, allelochemicals phenolics, and others, following Harborne (1977). Many of these compounds either play a role In common with other plants, grasses produce a in allelochemical interactions or act as feeding large array of secondary compounds that are not deterrents. 74 GRASSES AND GRASSLAND ECOLOGY
(a) (b)
HO CH3O O OH C N OH O HO C O HO C + HCN N O H O H Benzaldehyde OH CH2OH Glucose Dhurrin (c) Cyanohydrin + Glucose
CH3 O (d) HO CH2 CH NH C CH 3 (e) N H H CH CH COOH CH3 CH2 N CH3 N N H OH H
Figure 4.6 Some secondary compounds found in grasses: (a) DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one), a hydroxyamic acid; (b) dhurrin, a cyanogenic glycoside; during cyanogenesis, the molecule is hydrolysed to release hydrogen cyanide; (c) ergonovine, an ergot alkaloid; (d) paracoumaric acid, a phenol; (e) gramine, an indole alkaloid, derived from the aromatic amino acid typtophan. Reproduced with permission from Vicari and Bazely (1993).
palatability to sheep, although their concentra- 4.3.1 Nitrogen compounds tion decreases with plant age. Phalaris staggers is Nitrogen-containing secondary compounds a sometimes fatal condition in sheep due to alka- include the alkaloids, amines, non-protein amino loids in the tissues of P. tuberosa (harding grass) acids, cyanogenic glycosoides, and glucosi- and P. aquatica (bulbous canary grass) (Lee et al. nolates. Glucosinolates are largely restricted to 1956). The indole alkaloid gramine (Fig. 4.6) is pro- the Brassicaceae and are not considered further. duced in the youngest leaves of barley (Hordeum The non-protein amino acid ornithine has been vulgare) when grown under long photoperiods at reported from wheat (Triticum aestivum), where it high temperatures and acts as a feeding deterrent appears to act as a feeding deterrent to Sitobion to aphids and locusts (Ishikawa and Kanke 2000; avenae (grain aphid) (Ciepiela and Sempruch 1999); Salas and Corcuera 1991). Gramine and hordenine otherwise non-protein amino acids are more wide- have been extracted from the roots of H. vulgare spread in other plant groups such as the Fabaceae. act as allelochemicals reducing radicle length Alkaloids are based on one or more nitrogen- and general health and vigour in target species containing rings and include pharmaceutically (Sánchez-Moreiras et al. 2004). Fungal endophytes important compounds such as nicotine, atropine, when in mutualistic association with grasses strychnine, and quinine. These compounds can (Chapter 5) produce ergot (Fig. 4.6c) and other alka- have dramatic physiological effects on animals. loids. Graminivorous insects, especially aphids, Alkaloids are known from many grasses, especially are deterred from feeding on endophyte-infected the genera Festuca, Lolium, and Phalaris, particu- grasses because the alkaloid loline reduces insect larly in seedlings and plants under stress. These growth, survival, and fecundity. Fescue toxicosis chemicals act as feeding deterrents to grazers and and ryegrass staggers are serious conditions affect- allelochemicals. For example, indole alkaloids in ing large herbivores including cattle and horses Phalaris arundinacea (reed canary grass) reduce its when feeding on endophyte-infected Schedonorus PHYSIOLOGY 75 phoenix and Lolium perenne swards (Vicari and are derived from the geranyl pyrophosphate
Bazely 1993). In these infected grasses, ergopeptine pathways, and include mono- (C10), sesqui- (C15), alkaloids accumulate in the leaves, especially the di- (C20), and triterpenoids (C30). The immense vari- vasoconstrictive ergovaline and the tremorgenic ety of terpene compounds that can be built from neurotoxin lolitrem B (Gibson and Newman 2001). simple isoprene units include β-carotene (a vita- Amines are another class of nitrogen-containing min), natural and synthetic rubbers, plant essential molecules synthesized by the decarboxylation of oils (monoterpenoids such as citral in lemon), the amino acids or by transamination of aldehydes. plant growth regulators, abscisic acid (a sesquiter- The plant hormone idoleacetic acid is a tryptamine penoid), the gibberellins (diterpenoids), and steroid (tryptophane derivative) and several plants con- hormones (such as oestrogen and testosterone) in tain aromatic aliphatic amines in their flowers, animals. e.g. in the Araceae. Polyamines have been shown Terpenoids are not widespread in the grasses, to accumulate in response to developmental and although isoprene emissions of 0.02→40 µg g environmental signals (Bouchereau et al. 2000), (LDW)–1 h–1 are reported in Arundo donax, Chusquea including heat stress in rice (Oryza sativa) (Roy spp., Phragmites australis and P. mauritianum, and and Ghosh 1996) and salt stress in Bromus spp. Triticum aestivum, and monoterpenoid emissions (Gicquiaud et al. 2002). of <0.08–0.11 µg g (LDW)–1 h–1 in Chusquea spp., Cyanogenic glycosides, which consist of a nitrile Phragmites mauritianum, Secale cereale, Sorghum (triple-bonded CN), glucose (or other sugar), and a bicolor, and Triticum aestivum (Kesselmeier and variable R-group as part of the glucosinolate path- Staudt 1999; König et al. 1995). Emission of isoprene way, occur in c.3000 species of higher plants in 110 was reduced under elevated atmospheric CO2 in plant families. Cyanogenic glycosides are hydro- P. australis; this is thought to be due to inhibition of lysed through the removal of the glucose molecule the expression of isoprenoid synthesis genes and by β-glucosidase to release hydrogen cyanide (HCN, isoprene synthase activity (Scholefield et al. 2004). prussic acid) when tissue is damaged, e.g. through A variety of monoterpenes are reported in emis- maceration when grazed. Several forages contain sions from grassland vegetation. Examples include cyanogenic glycosides including the sorghums α- and β-pinene, myrcene, and limonene from a Sorghum spp. (which posses dhurrin, Fig. 4.6), Poa spp. dominated grassland in the Midwestern trefoils Lotus spp., and vetches Vicia spp. (Nelson USA (Fukui and Doskey 2000), and these plus and Moser 1994). Other grasses reported to contain α-thujene, camphene, sabinene, β-ocimene, and cyanogenic glycosides include Cynodon plectostach- γ-terpinene were reported in emissions from an yus (Vicari and Bazely 1993), Dendrocalamus gigan- Austrian grassland (König et al. 1995). However, teus (Ferreira et al. 1995), and Pennisetum purpureum the significance of these emissions for grassland (Njoku et al. 2004). Hydrogen cyanide is absorbed structure and composition is difficult to judge, as through the digestive tract of the grazing animal expected lifetimes with respect to oxidation by where it inhibits cytochrome oxidase in the respi- NO3 are only a few minutes. Terpenoids and other ratory electron transport chain. Levels of cyano- volatile organic compounds are of global impor- genic glycosides are highest in young leaf tissues tance as their oxidized products are involved in the and vary with plant age and growth conditions. formation of tropospheric ozone and other photo- chemically produced oxidants. The importance of terpenoids to grasses may 4.3.2 Terpenoids be as an indirect defensive chemical (Turlings The terpenoids (isoprenoids) are a large class et al. 1990). Corn Zea mays seedlings were found of volatile secondary compounds (>25 000 com- to release monoterpenes in response to saliva of pounds) based on five-carbon isoprene (C5H8) mol- Spodoptera exigua (beet armyworm) larvae. The par- ecules connected together. Each isoprene unit has asitic wasp Cotesia marginiventris was attracted to a ‘head’ and a ‘tail’ end, and isoprene blocks can be deposit its eggs into the caterpillars, thus defend- joined in many ways. Biosynthetically, terpenoids ing the corn against further predation. 76 GRASSES AND GRASSLAND ECOLOGY
Sesquiterpenoid cyclohexane derivatives Artificially synthesized in the laboratory since the such as blumenin (e.g. blumenol C, 9-O-(2′-O-β- late nineteenth century, courmarin is used to make glucuronosyl)-β-glucoside, structurally similar perfumes and flavourings, and in the preparation to abscisic acid) are widespread in mycorrhiza- of anticoagulants and rodenticide. Courmarin has infected grass roots, most frequently in the tribes been implicated to be involved in flowering, and Aveneae, Poeae, and Triticeae (Maier et al. 1997). inhibiting root development in Hordeum, tiller- The reason for this fungus-induced accumulation ing in Saccharum, and leaf elongation in Triticum of terpenoids is unclear; the chemicals may play a (Brown 1981). role in the physiological functions of mycorrhizal Quinones can be produced from phenols by fungi (see § 5.2.3), or could reflect a stress response enzymatic oxidation and are compounds with to fungal infection by the plant. The highest lev- either a 1,4-diketocyclohexa-2,5-dienoid (i.e. els of blumenin were reached 3–4 weeks after p-quinones) or a 1,2-diketocyclohexa-3,5-dienoid inoculation in the cortex of secondary roots of (o-quinones) moiety (Leistner 1981). These phe- wheat. Blumenin strongly inhibits fungal coloniza- nolics do not appear to be widespread in the tion, suggesting that these compounds might be grasses. Sorgoleone. for example, is found in involved in mycorrhizal regulation by the plant extracts and exudates of Sorghum bicolor where (Fester et al. 1999). in agricultural fields it acts as an allelochemi- cal reducing the growth of neighbouring weeds (Einhellig and Souza 1992; Sánchez-Moreiras 4.3.3 Phenolics et al. 2004). Mechanistically, sorgoleone acts as Phenolics are three-ring system compounds con- an inhibitor of photosynthetic electron transport structed from a cinnamic acid derivative and three (Nimbal et al. 1996). malonyl CoA molecules as an end product of the Flavonoids occur in most angiosperm families shikimic acid pathway. There are >500 types of as intensely coloured flower pigments, giving the phenolics in several structural classes includ- orange, red, purple, and blue colours to many ing aurones, flavones, anthocyanins, and tannins fruits, vegetables, flowers, leaves, roots, and stor- (polyphenolics). Phenolics occur in all vascular age organs. Chemically, flavonoids are polyphe- plants. Tannins are important feeding deter- nolic compounds possessing 15 carbon atoms; 2 rents in many plants, particularly woody plants, benzene rings joined by a linear 3-carbon chain. because of their astringency (reducing palatability) The chemical structure is based on a C15 skel- or indigestibility (protein-binding characteristics), eton with a heterocyclic chromane ring (C) bear- but are not present in the Poaceae and so are not ing a second aromatic ring (B) (Fig 4.7a). Ring C considered here. can occur in an isomeric open form or, more fre- The structurally simplest phenolics occur- quently, as a five-membered ring as shown in Fig ring in grasses are phenylpropanoids, e.g. caffeic, 4.7a. Ring B is most frequently in position 2 of the p-coumaric, ferulic, and sinapic acids are reported heterocylic ring C, although in isoflavonoids it from the leaves of >70 species of grass (Harborne occupies position 3. Over 4000 flavonoids are clas- and Williams 1986). These phenolics occur bound sified according to the substitution patterns and to cell-wall hemicellulose (p-coumaric, ferulic acid), oxidation state of the heterocyclic ring C, and the bound in the lipid fraction or linked to hydrocar- position of ring B. bon alcohols, fatty acids, or glycerol (caffeic and The six major chemical subgroups of flavonoids ferulic acids), or in leaf wax (p-hydroxybenzalde- are: chalcones (mostly intermediates in biosynthe- hyde in Sorghum bicolor) (Harborne and Williams si s of ot her f l avonoid s), f l avone s (ge nera l ly i n herba- 1986). When present in leaf wax they are related ceous families, e.g. Labiatae, Apiaceae, Asteraceae), to resistance to locust feeding. The familiar aroma flavonol (generally in woody angiosperms), fla- of freshly mown hay is due to the release of vanone, anthocyanins, and isoflavanoids (limited coumarin (1,2-benzopyrone) following the hydrol- mostly to the Fabaceae). Of these, anthocyanins ysis of melilotic acid (dihydro-o-courmaric acid). and flavones are considered further below. PHYSIOLOGY 77
(a) black appearance. Nevertheless, the anthocyanins commonly present in the angiosperms as a whole O B tend to predominate in the grasses too (i.e. cyani- A C din 3-glucoside—structurally the hydroxyl group
in the C3 ring in the flavylium skeleton (Fig. 4.7b), is replaced by a sugar). In the Pooideae and Panicoideae, the anthocy- OH anins contain aliphatic acyl groups (e.g. cya- (b) nidin 3-(3″,6″-dimalonylglucoside and other malonylyed cyanadin 3-glucosides), whereas in the HO O Ehrhartoideae, Bambusoideae, and Arundinoideae acylated anthocyanins are generally absent and a different pattern of 3-glucosides of cyanidin and OH peonidin occurs (Fossen et al. 2002). The anthocyanins in the cereals have been HO closely investigated (Escribano-Bailón et al. 2004). Figure 4.7 (a) The flavonoid skeleton; (b) the flavylium skeleton. At least six different anthocyanins have been identified from the cob of purple corn, a pig- mented variety of Zea mays. These anthocyanins Flavones (e.g. apigenin, luteolin, arthraxin) are occur in the epidermal cells and play a role in heavily oxidized structures based on the flavonoid protection against UV-B radiation and inhibition skeleton (Fig. 4.7a) as both glycosides and aglycones of alfatoxin production of by the fungal pathogen (i.e. whether bound to sugar or not). C-glycoside Aspergillus flavus. Cyanidin-3-glucoside, peono- flavones are characteristic of the grasses, occur- din-3-glucoside, and small quantities of several ring in 93% of species surveyed (Harborne and other anthocyanins have been identified from the Williams 1986). Tricin was first isolated from a husk of red and black rice grains. Commercially, rust-resistant wheat variety, and has subsequently the anthocyanin pigments are used as food col- been found to be common throughout the grass ourants, and, in the field, they inhibit growth of family despite its rarity in other plant groups Xanthomonas oryzae, one of the principal pathogens (Harborne 1967). Tricin extracts from brown rice of rice. Similarly, the pigmentation of blue, purple, bran are being investigated as a growth inhibitor and red wheat (Triticum aestivum cultivars) is due of human breast and colon cancer (Cai et al. 2004; to the accumulation of anthocyanins, including Hudson et al. 2000). glucosides and rutinosides, and acylated deriva- Anthocyanins are based on addition or removal tives of cyanidin and peonidin. Sorghum S. bicolor of hydroxyl groups or by methylation or glyco- is one of the few monocotyledons that synthesizes sylation of a flavylium (2-phenylbenzopyrilium) antimicrobial phytoalexins in response to patho- skeleton (Fig. 4.7b) (Escribano-Bailón et al. 2004). gen infection. The phytoalexins of sorghum are Anthocyanidins (aglycon) are formed when the pigmented 3-deoxyanthocyanidins, which accu- flavylium skeleton is united with one or various mulate in cellular vesicles around the area in the sugars, which in turn can be acylated with an cells under fungal attack. organic acid. The functional significance of flavonoids in Anthocyanins are intensely coloured and the grasses is also related to grazing deterrence, pri- most important class of pigments responsible marily for insects. For example, the wheat cultivar for pink, scarlet, red, mauve, violet, and blue Amigo is avoided by the aphid Schizaphis graminum colours in petals and leaves of higher plants because of the presence of tricin and glycosylfla- (Harborne 1967). In grasses, this pigmentation is vones in the leaves (Harborne and Williams 1986). often obscured by admixture with plastid pig- Other grass flavonoids act as feeding attractants and ments (chlorophylls), leading to a brown, grey, or can even be sequestered and stored in the insect. 78 GRASSES AND GRASSLAND ECOLOGY
For example, 1–2% of the body and wing dry weight effectiveness of hydroxamic acids against vertebrate of the butterfly Melanargia galathea can be sequses- herbivores is unknown. DIBOA, DIMBOA, and tered flavones (hydrolysed tricin 7-glucoside). There other hydroxamic acids have been identified from is some evidence of feeding selection in mammals root extracts as allelochemicals inhibiting seed being due to phenolic levels in grass tissues, but germination and growth from Elymus repens, Secale apart from some weakly oestrogenic effect, flavo- cereale, Triticum aestivum, T. speltoides, and Zea mays noids do not appear to affect animal reproduction (Sánchez-Moreiras et al. 2004). (Harborne and Williams 1986). An exception might be the mountain vole Microtus montanus, which 4.4 Silicon ingests high concentrations of p-courmaric and caffeic acids from Distichlis stricta, which inhibits Silicon is the second most abundant element in winter breeding. the soil, and, in quartz and other minerals, the Flavonoids play an important role in the attenua- substrate for most of the world’s plant life. In the tion of solar UV-B radiation mitigating leaf damage soil solution silicon occurs mainly as silicic acid,
(Bassman 2004). Synthesis of flavonoids and other H4SiO4, at 0.1–0.6 mM concentrations similar to phenolics is due to induced gene expression for the that of potassium, calcium, and other major plant key biosynthetic enzymes. For example, synthesis nutrients (Epstein 1994). Silicon is readily absorbed of hydroxycinnamates (phenolics) was induced by by forages with water as Si(OH)4 where it can UV-B in Hordeum vulgare. By enhancing second- reach concentrations in the plant up to 10% of dry ary plant metabolites and thereby affecting plant– matter. The normal range in the foliage of forage herbivore and plant–pathogen interactions, it is plants is 400–10 000 mg kg–1 (Barker and Collins postulated that UV-B radiation is an important 2003). Plants which contain >1% silicon and have a mediator of multiple trophic interactions in terres- silicon/calcium molecular ratio >1 are referred to as trial plant communities (Bassman 2004). silicon accumulators (Ma et al. 2001), of which the grasses predominate. Soluble silicon concentration reaches a maximum at a soil pH of 8–9 (Prychid 4.3.4 Other compounds et al. 2003). Hydroxamic acids (4-hydroxy-1,4-benzoxazin- In the plant, silicon is irreversibly precipitated
3-ones) are derivatives of the shikimic acid bio- as amorphous silica (SiO2-nH2O or ‘opal’ or silica synthetic pathway and occur in a wide variety of gel) in phytoliths. In grasses, phytoliths occur in grasses, including cereal crops, maize, barley, wheat, the epidermis and subepidermal sclerenchyma of and some wild grasses (Deschampsia spp., Elymus most species. Silica bodies are morphologically spp., Hordeum spp.,and Phalaris spp.), mainly in the diverse in the Poaceae, including dumbbell-shaped, Triticeae tribe (Gianoli and Niemeyer 1998; Vicari cross-shaped, saddle-shaped, conical-shaped, and and Bazely 1993). The main compounds include horizontally elongated bodies with smooth or sinu- DIMBOA (2,4-dihydroxy-7-methoxy-1,4-benzox- ous outlines. Silica bodies are abundant in some azin-3-one, Fig. 4.6) and DIBOA (2,4-dihydroxy-1, tissues and can occur as dust particles from plant 4-benzoxazin-3-one) inhibitors of mitochondrial fragments in the atmosphere where they have been metabolism and an inducible defence. Levels found to be carcinogenic. For example, Phalaris increase following leaf damage and deter her- species contain high levels of silica bodies in inflo- bivorous chewing and sap-sucking insects, and rescence bracts. These grasses are known contami- bacterial and fungal pathogens. Highest levels nants of cereal crops of north-east Iran where there occur in seedlings, with concentrations declin- is also a high incidence of oesophageal cancer ing with age. In perennials, concentrations vary (Sangster et al. 1983). seasonally, with maximum levels occurring in the Although silicon is not regarded as an essential summer coinciding with the peak of insect herbiv- element (§ 4.2.1), this view is increasingly being ory. Breeding programmes have been established to questioned (Epstein 1994, 1999; Richmond and increase hydroxamic acid levels in cereal crops. The Sussman 2003). The benefits of silicon to plants PHYSIOLOGY 79 include improved resistance to pathogens and are able to grow semi-autonomously while remain- herbivory, maintenance of stem and leaf rigid- ing physically attached to the mother plant reflects ity, reduced leaf transpiration through improved mechanisms of ramet regulation, especially the water use efficiency, and tolerance of drought and degree of physiological integration among mod- heavy metals (Richmond and Sussman 2003). The ules. Morphologically there is a continuum of clonal ‘window’ hypothesis suggests that epidermal silica growth forms ranging from ‘phalanx’ growth bodies facilitate the transmission of light through forms with tightly clumped tillers (e.g. bunch- the epidermis to the photosynthetic mesophyll or grasses such as Festuca ovina and Schizachyrium to stem cortical tissue, increasing photosynthesis scoparium) to ‘guerrilla’ forms with widely spread- and plant growth. However, this hypothesis does ing rhizomes (e.g. Cynodon dactylon) (Lovett Doust not appear to have been supported by experimental 1981). No matter what the growth form, all or a studies (Agarie et al. 1996; Prychid et al. 2003). Silica subset of the rhizomes in a clone may constitute bodies in the leaf epidermis do, however, confer an integrated physiological unit (IPU) in which resistance to UV-B radiation damage as a result resources (nutrients, photosynthates, water) may of an increase of phenolic compounds induced by be transferred back and forth. Integration among silicon (Li et al. 2004). ramets in this manner allows for (1) equitable dis- The role of silicon in the ecology and co-evolution tribution of resources among ramets, (2) minimal of grazed grassland ecosystems may be consid- inter-ramet competition, and (3) optimal efficiency erable (see Chapter 2). Studies in the African of resource acquisition (Briske and Derner 1998). It Serengeti showed high concentrations of tissue has been suggested that high levels of physiological silicon (averaging 19.6% from a heavily grazed integration would allow compensatory growth fol- site, 11.9% from a less grazed site) that decreased lowing partial defoliation under grazing. However, through the growing season and from the roots support for the compensatory growth hypothesis to the leaves (McNaughton et al. 1985). In a labo- was not found in a study of Digitaria macroblephara ratory experiment, silicon promoted growth of and Cynodon plectostachyus in the Serengeti (Wilsey unclipped native grasses and increased leaf chlo- 2002). Although severed rhizomes produced less rophyll content. The authors suggested that natu- biomass than unsevered rhizomes, supporting the ral selection for silicon accumulation was related idea that physiological integration may be impor- to grazing exposure. Silicon acts as a defence tant, this decrease was independent of defoliation. against herbivory by facilitating abrasion of the By contrast, physiological integration was found to mouthparts of herbivores, thus protecting vul- help ramets of Psammochloa villosa survive burial nerable plant tissues. Silicon concentrations >2% in a sand dune habitat (Yu et al. 2004). Resources can also lead to fatal silica urolithiasis in bovine transferred from unburied ramets increased the calves. In addition, silicon deposition in tissues ability of buried ramets to elongate and grow to may improve the carbon and energy economy of the surface. grasses by releasing carbon that would otherwise The degree of physiological integration was go into secondary thickening and stiffening of the investigated in the clonal perennial Panicum virga- plant. tum (Hartnett 1993). Clones of P. virgatum growing in North American tallgrass prairie were subjected 4.5 Physiological integration of to combinations of nutrient addition, neighbouring clonal grasses and mechanisms of plant removal, and rhizome- severing treatments. ramet regulation There was no effect of rhizome severing or inter- action with the other treatments indicating that The diverse modular morphology allowing tillering the integrated physiological unit was smaller than and clonal growth that characterizes many grasses clone size or unrelated to the treatments. Thus, in affords the opportunity to forage and explore the P. virgatum, transfer of resources among ramets local environment (Chapter 3). The extent to which may either be short-term or limited to small sub- ramets of grasses and other similar clonal plants sets of ramets within the clone. 80 GRASSES AND GRASSLAND ECOLOGY
Figure 4.8 Clones of cespitose grasses organized as assemblages of autonomous ramet hierarchies, rather than as a sequence of integrated ramets. The benefits of physiological integration are restricted to individual ramet hierarchies (solid circles), while interhierarchical competition occurs for soil resources beneath the clone as a whole (dashed circle). Reproduced with permission from Briske and Derner (1998).
The study of P. virgatum (Hartnett 1993) out- Ramet regulation and hence new tiller recruit- lined above, along with other studies (reviewed ment in clonal grasses is under complex physi- in Briske and Derner 1998) indicate that complete ological and ecological control. Tomlinson and physiological integration among ramets in a clonal O’Connor (2004) suggest an integrated model in grass is normally limited to young plants. Rather, which bud release for new tillers in controlled by physiological integration is confined to sets of the auxin:cytokinin ratio. Red:far-red light ratios individual ramet hierarchies (groups of ramets) (a consequence of the local light environment) (Fig. 4.8). Part of the breakdown in physiological affect production and export of auxin from shoots, integration among ramets is due to disruption of whereas root nitrogen concentration (itself affected vascular continuity among ramets in older clones. by soil resources) affects cytokinin production. Mycorrhizal connections among roots of neigh- Thus, shifts in local soil nitrogen and the shoot’s bouring ramet hierarchies may allow low levels of light environment interact to control the produc- resource reallocation. tion of new tillers. CHAPTER 5 Population ecology
There can be therefore little doubt that this plant gen- (particularly daylength). Classic experiments by erally propagates itself throughout an immense area by Calvin McMillan (1956a, 1956b, 1957, 1959b) showed cleistogamic seeds, and that it can hardly ever be invig- substantial ecotypic variation in flowering time for orated by cross-fertilization. It resembles in this respect the dominant grasses across the North American those plants which are now widely spread, though they Great Plains (see § 5.3 for discussion of ecotypes). increase solely by asexual generation. Yearly fluctuations in temperature and soil mois- Charles Darwin (1877), commenting on ture can affect the timing of flowering, even in rice cutgrass Leersia oryzoides populations otherwise genetically constrained to a daylength response. A good example is the genetic Population ecology seeks to understand the rela- differentiation and phenotypic plasticity in flower- tionship between groups of individuals of a single ing phenology illustrated by the perennial bunch- species in an area (a population) and their envi- grass Notodanthonia caespitosa in southern Australia. ronment. The ‘father’ of plant population ecology Flowering in southern populations growing in was John L. Harper, following the publication of cool, moist temperate environments was closely his Population Biology of Plants in 1977, and, indeed, tied into daylength responses related to a relatively much of his work was undertaken in a Lolium per- predictable growing season. By contrast, northern enne–Trifolium repens sheep pasture in North Wales populations growing in hot, semi-arid conditions (e.g. Sackville Hamilton and Harper 1989; Sarukhán are frequently exposed to daylengths exceeding the and Harper 1973; Turkington and Harper 1979). critical value for floral initiation so that once flow- Many topics in the population ecology of grasses ering tillers form, temperature and soil moisture and grasslands are covered in the book edited by determine the rate of reproductive development G.P. Cheplick (1998a) (see review in Gibson 1998). (Quinn 2000). Similarly, populations of Danthonia In this chapter, some of these important topics sericea in the north-eastern USA growing in wet are explored. First, reproduction and population habitats flowered in response to substrate tem- growth of grasses is discussed (§ 5.1), followed by perature, whereas populations from well-drained a discussion of how fungi infecting grasses either upland soils required an additional photoperiod above or below ground affect their population stimulus (Rotsettis et al. 1972). ecology (§ 5.2), and finally, ecotypes, polyploidy, Prior exposure to low temperatures is necessary hybridization, and genetic structure are covered to initiate flowering in many grasses, especially under the heading of genecology (§ 5.3). festucoid perennials from temperate zones, even under favourable daylengths. This requirement 5.1 Reproduction and population is referred to as vernalization, and is necessary dynamics every year in perennials. Vernalization tempera- tures range from –6 °C to c.14 °C. The vernalization 5.1.1 Flowering phenology requirement varies among species and cultivars The timing of flowering (i.e. phenology) in grasses within species. For example, within Poa, P. alpina is under genetic and environmental control and P. pratensis have an obligate vernalization
81 82 GRASSES AND GRASSLAND ECOLOGY requirement, P. bulbosa and P. palustris respond the egg to form the diploid (2n) zygote. The other to vernalization, but P. annua shows no response sperm nuclei fuse with the two polar nuclei to form (Evans 1964). the triploid (3n) endosperm. Exceptional instances of single fertilization in which the caryopsis has normal endosperm but no embryos are reported 5.1.2 Anthesis and pollen dispersal for wheat (Evans 1964). Lodicules in the floret inflate, forcing apart the palea and lemma, allowing the anthers to protrude Cross- and self-incompatibility and pollen to be shed. Generally, species are either The control of compatibility in grasses is appar- morning or afternoon flowering, with some species ently unique and based on the rejection of self- being nocturnal. For example, Prokudin (in Conner pollen on the stigmatic surface. Control is enabled
1986) reported flowering in Poa spp. from the same through two polyallelic, unlinked loci, S1,2,3 . . . , and site at 8 a.m.–12 noon for P. sterilis, 5–8 p.m. for Z1,2,3 . . . . A diploid grass possesses two S and two
P. nemoralis, and 11 p.m.–12 midnight for five other Z alleles, e.g. S1S2Z1Z2, whereas haploid pollen has
Poa spp. one allele from each gene, e.g. S1Z2. There are tens Grass pollen is predominantly anemophil- of alleles for each gene, allowing hundreds of com- ous (wind pollinated). Entomophily (insect pol- binations of alleles of the two genes. Rejection of lination) is restricted, for the most part, to a few pollen occurs when alleles of the haploid pollen tropical grasses (e.g. Olyra, Pariana; Soderstrom matches those of the diploid sporophytic stigma; and Calderón 1971). For example, honeybees Apis the two must share no alleles to be compatible. cerana were observed to collect pollen and facilitate Thus, a pollen parent S1S2Z1Z2, would give rise to pollen release in the bamboo Phyllostachys nidularia pollen S1Z1, S1Z2, S2Z1, S2Z2, all of which would fail
(Huang et al. 2002). There are a few observations of if landing on a style of genotype S1S2Z1Z2. By con- entomophily in temperate grasses; for example, pol- trast, a pollen parent S1S3Z1Z3 would give rise to lination by solitary bees (Halictidae) was observed S1Z1, S1Z3, S3Z1, and S3Z3 pollen of which a quarter to significantly enhance seed set in Paspalum dila- fails on the S1S2Z1Z2 style (i.e. S1Z1 genotype fails) tatum (Adams et al. 1981). In both cases, the pollen/ (Chapman 1996). The incompatibility reaction is ovule ratio was low and in P. dilatatum the pollen retained in polyploids (§ 5.3). Inhibition of incom- was larger than usual for anemophilous species patible pollen occurs after the pollen tube tip con- and dispersed as clusters of grains. tacts the stigma, and can take place within as little Despite being predominantly wind dispersed, as 2 minutes of first contact (Heslop-Harrison and grass pollen often does not travel very far. More Heslop-Harrison 1986). than >90% of the pollen was dispersed within 5 m in Pennisetum glaucum, and Zea mays, although in 5.1.3 Breeding systems Lolium perenne and Phleum pretense >20% travelled >200 m (Richards 1990). There is a wide array of breeding systems in the The pollen is captured among trichomes on the grasses, from hermaphroditism to dioecism. stigma, where the grain begins to hydrate imme- Perennial grasses are mostly cross-fertile and diately. Germination proceeds as the pollen tube partially or totally self-fertile. Annual grasses are emerges through the pore of the pollen grain and mainly self-fertile (Gould and Shaw 1983). In some grows into the stigma. A vegetative nucleus is genera there appear to be evolutionary trends from located at the tip of the pollen tube, followed by self-incompatible perennials to self-pollinated two sperm nuclei. Passage of the pollen tube nuclei annuals (e.g. in Bromus, Hordeum, Elymus, Agropyron, to the ovary can be complete within an hour in Festuca, and Poa) (Stebbins 1957). Mechanisms wheat, or take as long as 22 hours in maize with its to ensure cross-fertilization include late bloom- long silks (Chapman and Peat 1992). Double ferti- ing of male spikelets compared with hermaph- lization characteristic of the angiosperms involves rodite spikelets in polygamous species in tribes union of one of the haploid (1n) sperm nuclei with such as Andropogoneae and Paniceae. Entirely POPULATION ECOLOGY 83
hermaphroditic taxa may be proterogynous with the as a breeding system offers an advantage of effi- anthers protruding and releasing pollen before the cient and successful pollination, which can enhance stigmas are visible (e.g. Alopecurus, Anthoxanthum, fecundity (seed production). For example, plants of Pennisetum, Spartina). Environmental conditions Dichanthelium clandestinum were noted to produce can modify the mating system, shifting the balance c.10 times the number of cleistogamous as chas- between self-fertilization and cross-fertilization. mogamous (open-flowered) seeds with c.4 times For example, frost can emasculate wheat and bar- greater recruitment of cleistogamous-derived seed ley ensuring outbreeding (Evans 1964). in the field (Bell and Quinn 1985). An extreme form Some self-fertile grasses produce cleistogamous of cleistogamy is amphicarpy in which modified flowers in which pollination occurs in closed flo- cleistogamous spikelets are borne on underground rets; e.g. Sporobolus cryptandrus where terminal tillers, e.g. Amphicarpum purshii, A. muhlenber- spikelets remain partially or totally enclosed in gianum, Enteropogon chlorideus. The resulting sub- the uppermost leaf sheaths. In S. vaginiflorus and terranean seed production in amphicarpic species some other annuals, lateral cleistogamous spikelets can provide a safe haven from above-ground dis- are produced late in the flowering season. Darwin turbances for the plants. For example, placement of (1877) noted the occurrence of cleistogamy in three seeds below ground in A. purshii provides protec- grass genera (Hordeum, Leersia, and Sporobolus) in tion from fire in frequently burned Pine Barrens a survey of this phenomenon. Nowadays, cleisto- habitats of New Jersey, USA (Cheplick and Quinn gamy is reported from 321 grass species from 82 1987). In this species, survival and fitness of seed- genera in all the subfamilies, being most common lings derived from cleistogamous seed was much in the advanced Panicoideae and in temperate greater than seedlings from the aerial chasmoga- zones of the New World (Campbell et al. 1983). The mous seed (Cheplick and Quinn 1983, 1987). The genus with the largest number of cleistogamous mixed mating system, in which seeds are pro- species is Stipa with 46. duced from spikelets borne either above or below A specialized type of cleistogamy is illustrated ground, helps maintain genotypic and phenotypic by the presence of dimorphic axillary cleistogenes plasticity (Cheplick and Quinn 1986). (cleistogamous spikelets enclosed by leaf sheaths on the lowermost culm nodes) in at least 22 species Asexual reproduction from 10 genera: Calyptochloa, Cleistochloa, Cottea, Apomixis is reproduction in sexual structures Danthonia (7 species), Enneapogon, Muhlenbergia, without actual fusion of male and female gametes. Pappophorum, Sieglingia, Stipa, and Triplasis Apomixis in grasses is either facultative or obligate. (Campbell et al. 1983; Chase 1908, 1918). In these spe- Facultative apomicts can produce offspring both cies the axillary seeds are not dispersed, remain- sexually and asexually. Obligate apomicts have lost ing within the leaf sheaths until the flowering tiller the capacity for sexual reproduction. An advan- senescences. The resulting seed heteromorphism tage of apomixis is that individuals can live to a represents an ecological ‘bet hedging’ strategy for great age and cover a large area (Richards 2003). plants. For example, the large, relatively heavy seed Apomixis is well represented in the grasses (in 62 produced from the low cleistogamous spikelets in genera, Czapik 2000), as well as other angiosperms, Triplasis purpurea can become buried by sand close especially the Asteraceae and Rosaceae. There are to the parent plant in the coastal habitat where two classes of apomixis: vivipary in which prog- this species occurs. By contrast, the smaller, 64% eny are produced other than by seed, and aga- lighter, seed produced by chasmogamous spikelets mospermy in which reproduction is by seed. In in the upper culms is wind dispersed across the apomictic vivipary, the reproductive structures sand surface (Cheplick and Grandstaff 1997). (e.g. flowers, lemmas, paleas) are transformed or As an evolutionarily derived feature, cleistogamy replaced by bulbils or bulblets; it is found in spe- has a genetic basis, but its occurrence is also influ- cies of Poa, Festuca, Deschampsia, and Agrostis. This enced by environmental factors including photope- form of vivipary (i.e. pseudovivipary) is frequent riod, soil moisture, and temperature. Cleistogamy in grasses of alpine and arctic habitats (e.g. Poa 84 GRASSES AND GRASSLAND ECOLOGY alpina var. vivipara, Festuca viviparoidea) some arid an embryo by mitotic division of the egg cell with- habitats (e.g.. Poa bulbosa, P. sinaica) (see annotated out fertilization; and may (pseudogamous) or may list in Beetle 1980), and environments of large spa- not (autonomous) require pollination. If pseudog- tial and temporal heterogeneity (Elmqvist and Cox amy, then the male gamete is required for develop- 1996). This is in contrast to true vivipary, found ment of the endosperm and embryo, but does not most frequently in species such as seagrasses and fertilize the ovule. mangroves inhabiting shallow marine environ- Agamospermy is most frequent in the Paniceae ments, which involves sexually produced offspring and Andropogoneae compared with other grass with the embryo penetrating the fruit pericarp tribes (Brown and Emery 1958); examples include and growing to considerable size before dispersal Poa artica, P. alpigena, P. alpina, and P. pratensis (Elmqvist and Cox 1996). Proliferation is some- which are parthenogenetic and pseudogamous times referred to as a form of vivipary but involves (Evans 1946). Agamospermous apomicts of Poa the conversion of spikelets above the glumes into a species were found to be more successful than leaf shoot (see discussion in § 3.3). amphimicts (i.e. seed produced through fusion of The ecological advantage of pseudovivipary male and female gametes) in more exposed ter- in grasses as a reproductive strategy may be in rain, and in cool environments with short frost- allowing plants to reproduce quickly in the short free seasons (Soreng 2000). It is postulated that growing season of arctic, alpine, and arid environ- apomicts are better able than amphimicts to ments (Lee and Harmer 1980). These environments migrate and colonize new areas because apomicts are coarse-grained, with parental patches offering are not limited reproductively with the need to the best opportunity for establishment of offspring find a mate (pollen). Thus, apomicts appear to be in both time and space. Potential benefits of pseu- more opportunistic and r-selected than their sex- dovivipary include: the size advantage of bulbils ual counterparts. allowing carryover of nutrients and organic matter to the next generation; continuous growth without Dioecy changing form or energy loss from mobilization The presence of two sex forms in populations, one and redistribution of reserves for seed production; pistillate and seed bearing (i.e. female), and the leaves being ready for assimilation immediately other staminate and pollen producing (i.e. male) is even before dispersal; avoidance of nutrient loss known as dioecy (dioecious from Greek di (two) + from pollen production; and a likely high estab- oikos (housed) + ous). Dioecious grasses occur lishment probability for propagules. Limitations with highest frequency in the continental New are those for all forms of apomixis and include World, especially Mesoamerica. Dioecious genera restricted genetic exchange and the potentially high occur in 5 tribes: Arundineae: Gynerium (1 dioe- energy costs in producing the sometimes large veg- cious species); Chlorideae: Buchloe (1), Buchlomimus etative plantlets. Some species are semi-viviparous, (1), Cyclostachya (1), Opizia (2 or 3), Pringleochloa (1), producing both viable seed and viviparous prop- Soderstromia (1); Eragrostideae: Allolepis (1), Distichlis agules (e.g. Festuca viviparoidea). (13), Jouvea (2), Monanthochloe (3), Neeragrostis (2), There are two sorts of agamospermy: Reederochloa (1), Scleropogon (1), Sohnsia (1); Paniceae: ● Adventitious embryony has been reported in Pseudochaetochloa (1), Spinifex (4), Zygochloa (1), Poa and occurs when the embryo arises in the Poeae: Festuca (400), Poa (500) (Connor et al. 2000). ovule but outside the embryo sac in the nucellus or In most populations that have been observed the integument and the new sporophyte arises directly expected 1:1 male:female sex ratio occurs (Connor from sporophyte tissue without a gametophyte; et al. 2000). The evolutionary advantage of dioecy alternation of generations is thus avoided. appears to be one of an outcrossing advantage ● Gametophytic apomixis occurs when a 2n game- (avoidance of inbreeding) as niche specialization tophyte is produced without reduction division and of males vs females or comparative differences fertilization; e.g. parthenogenesis, the formation of in fitness appear to be lacking (Quinn 1991). POPULATION ECOLOGY 85
Nevertheless, spatial segregation of the sexes has A survey of 1725 seedbank studies (45% from been observed in some grasses, e.g. Distichlis spi- grasslands) from north-west Europe recorded 130 cata (more females in saline areas) and Hesperochloa of 241 possible grass species known for the region, kingii (more females at wetter sites) (Bierzychudek with 2033 of 4237 (49%) records being for transient and Eckhart 1988). As noted above, this does not species (Thompson et al. 1997). Twenty-two grasses necessarily demonstrate niche partitioning among were included in the top 100 species ranked by the sexes; alternative explanations, such as dif- number of records in the database of which Holcus ferential mortality, parental determination of off- lanatus, Poa trivialis, Poa pratensis, and Festuca rubra spring sex ratios, or environmentally determined were ranked in the top 10 (3rd, 5th, 8th, and 9th, sex change, may be more likely (Fox and Harrison respectively). Seed density varied by species and 1981). For Distichlis spicata, sex is genetically deter- depth of sampling. The 5 grasses with the highest mined and gender-specific bias in seedling survi- mean density in the top 10 cm of soil were Bromus vorship appears to be a causal factor in determing hordeaceus (18 110 seeds m–2), Glyceria fluitans (17 957 the sex ratio in specific microsites (Eppley 2001). seeds m–2), Lolium multiflorum (11 200 seeds m–2), Poa trivialis (6479 seeds m–2), and Alopecurus genicu- latus (6023 seeds m–2). 5.1.4 Seed banks, seed dormancy and Despite the apparent longevity of persistent seed germination, seedling establishment banks, few grass seeds are still alive after 5 years The morphology of the grass seed as it relates to of burial in the soil, although experimental stud- dispersal and the resulting seedling were described ies have reported a small percentage of seed living in § 3.7. It is important now to discuss how seeds for longer periods (e.g. 0.3–2.0% of Poa pratensis, accumulate in the soil, go through dormancy, ger- Setaria glauca, S. verticillata, S. viridis and Sporobolus minate, and grow as seedlings. cryptandrus alive after 39 years; Toole and Brown The seed bank represents the accumulation of 1946). Longevity of seeds of Agrostis capillaris seeds in (on) the soil. Seeds (defined very gener- has been reported as >40 years (Thompson et al. ally to include both seeds and fruits in this context) 1997). In nature, seeds are lost from the persistent of an individual species can form a transient seed seed bank through in situ germination, predation, bank if they live only until the first germination pathogens, or ageing (Fig. 5.1). Mortality follows season following maturation, or form a persist- a Deevey type II or negative exponential curve ent seed bank if they live until the second (or (indicating little age-related mortality), whereas subsequent) germination season (Thompson and seed in transient seed banks exhibit a much more Grime 1979). For example, California annual grass- rapid initial mortality closer to a Deevey type III lands were observed to possess only a transient curve (Baskin and Baskin 1998). An experimental seed bank. Few germinable seeds were carried study in native bunchgrass prairie of Oregon, USA, over from one year to the next and the dominant showed 44–80% of seeds from four species dying grasses had virtually no carryover (Young et al. within 1 year, with mortality due to three control- 1980). Persistent seeds banks, however, allow the led treatments—senescence, disease or vertebrate seeds produced by the vegetation to build up in the herbivory—being low (Clark and Wilson 2003). It soil. A survey of the literature revealed 61 genera was postulated that the probable causative agents and 99 species of grasses forming persistent seed of most mortality were non-fungal disease (bacte- banks at a density ranging from 1 (Digitaria ischae- ria and viruses), invertebrate predation, competi- mum, Hesperostipa comata, Hordeum vulgare, Sitanion tion, and abiotic constraints. hystrix) to 9340 (Zoysia japonica) seeds m–2 (Baskin The seed bank represents the living ‘memory’ and Baskin 1998). Another survey revealed grasses of the plant community and the species present as a group ranging in density from 7 (a mixed- include many that grew under previous environ- grass prairie) to 18 050 (annual grassland) seeds mental conditions, especially disturbances. As m–2 (total seed bank densities 287–27 400 seeds m–2 such, the seed bank provides a buffer against spe- respectively in these two grasslands) (Rice 1989). cies fluctuations and the risk of local extinction, 86 GRASSES AND GRASSLAND ECOLOGY
Germination Lives Light Mother plant D Die Germination Dies Seeds is not possible Eaten Seeds to Living seeds surface buried (could be D, Predators CD or ND) Seed CD CD Pathogens death
Ageing
Germination
is possible No germination in darkness ND Shoot grows to soil surface Shoot grows Shoot does not grow to soil surface Shoot does not grow
Germinate in darkness
Figure 5.1 General scheme showing factors affecting persistence and depletion of buried seeds of grasses and possible annual changes in dormancy state. D, dormant; CD, conditional dormancy; ND, non-dormant. Reproduced with permission from Baskin and Baskin (1998). and influences population recovery after distur- the composition of the seed bank can greatly influ- bance. In undisturbed North American prairie, few ence the species composition in early succession of the dominant perennial grasses or forbs occur following a disturbance. Regrowth from vegeta- in the persistent seed bank (Abrams 1988). With tive parts of the dominant species (the bud bank) a density of >6000 seeds m–2 in the top 12 cm of can, however, be more important than recruitment soil, the prairie seed bank is comprised mostly of from the seed bank (Benson et al. 2004; Virágh short-lived opportunistic species exhibiting a ‘sit- and Gerencsér 1988). Nevertheless, the composi- and-wait’ strategy, awaiting suitable conditions for tion of grassland seed banks is generally reflec- germination (Hartnett and Keeler 1995). In other tive of disturbances and management regimes grasslands, large differences between the com- (e.g. Kalamees and Zobel 1998; López-Mariño et al. position of the seed bank and the vegetation are 2000), such as rate of nitrogen addition (Kitajima frequently observed, principally due to the large and Tilman 1996). The similarity between the seed numbers of ruderal, ‘weedy’ taxa in the seed bank. bank and vegetation can be complex. For example, Indeed, the dominant species in the vegetation a study of Mediterranean grassland showed that can be absent from the seed bank. Lolium perenne the similarity between the vegetation and seed and Dactylis glomerata, often dominant in pastures, bank declined with increasing altitude but was are poorly represented in the seed bank, whereas unrelated to topography and grazing (Peco et al. Agrostis spp. and Poa spp. may have extensive seed 1998). In species-rich grassland, the number of spe- bank reserves (Rice 1989). Generally, annuals are cies represented in the seed bank can be few rela- better represented in grassland seed banks than tive to the vegetation, indicating that most of the perennials, and forbs are better represented than species are transient or that seed production is low grasses. The presence of ruderal species means that (Kalamees and Zobel 1998; O’Connor and Everson POPULATION ECOLOGY 87
1998). In wet semi-natural grassland in Sweden, a by plants, grass seeds have non-deep physiologi- species-rich seed bank appeared to contribute lit- cal dormancy (PD), i.e. dormancy can be broken tle to regeneration of the grassland (Milberg 1993). or stimulated by dry storage at room temperature, Seedling establishment was rare in undisturbed mechanical injury and/or removal of palea and vegetation, occurring most frequently in gaps from lemma, or gibberellic acid (GA3). Grasses thus lack the recent seed rain. Either way, the number of spe- morphological or physical dormancy. Some grasses cies in the vegetation is generally positively related are stimulated to germinate by any one of these to the number of species in the seed bank. conditions (e.g. Schizachyrium scoparium), whereas The use of the seed bank in grassland restora- others respond to only one of these conditions tion has been suggested. However, although some (e.g. Cynodon dactylon has PD broken only by dry species may be recruited into restoration from storage). For a grass seed to become part of the the seed bank, others may have to be naturally persistent seed bank it must be in a state of innate or artificially introduced for a successful restora- dormancy or enter secondary dormancy. In some tion (Bekker et al. 1997; Milberg 1995). For example, grasslands there is little evidence of either, e.g. per- Bossuyt and Hermy (2003) reviewed data from 16 ennial grasses of the sub-Saharan African savan- separate studies and noted a decline in total seed nahs (O’Connor and Everson 1998). Seed of other density with increasing age since abandonment grasses that are non-dormant when fresh include of traditional grazing or hay-cutting management some winter annuals and summer annuals, and of European grassland and heathland communi- perennials, e.g. Avena fatua, Milium effusum (Baskin ties, especially calcareous or alluvial grasslands. and Baskin 1998). Seeds of target species declined with time, and Dormancy-breaking requirements in grasses fall non-target ruderal or competitive agricultural spe- into two categories: high summer temperatures cies increased. Similar observations were made by or low winter temperatures (Baskin and Baskin Hutchings and Booth (1996) in a study of calcar- 1998). High summer temperatures are required eous grassland. By contrast, the accumulation of to break dormancy in winter annuals in temper- seed in a persistent seed bank can make the eradi- ate or Mediterranean climates, and perennials in cation or control of invasive species difficult. For Mediterranean or tropical-temperate climates, e.g. Poa example, Microstegium vimineum is an annual grass annua, Bromus tectorum, Aira praecox, Vulpia bromoides . of Asian origin invasive in the forest understory of Low temperatures are required for summer annual the eastern USA. It has been estimated to possess grasses and perennial grasses in temperate regions a persistent seed bank of 64 seeds m–2 in the top with dormancy breaking during cold stratification. 5 cm of soil under patches of flowering individuals When first under conditional dormancy, germina- (Gibson et al. 2002). tion is possible only at high temperatures (autumn temperatures are too low). Later, when non-dormant, Seed dormancy and germination winter germination occurs under a wide range of Except where attribution to other authors is indi- temperatures; example perennials include Dactylis cated, the examples of species exhibiting different glomerata, Festuca ovina, Panicum virgatum, Poa prat- dormancy and germination characteristics in the ensis, and Sorghastrum nutans, and annuals include following discussion are selected from the longer Setaria glauca and S. viridis. lists provided by Baskin and Baskin (1998). Seed When in a non-dormant state, germination dormancy is the inability of fresh mature seed to requirements depend upon an often complex germinate and is very common in the Poaceae. interaction of environmental factors. The principal Grass seeds pass through a transition of stages as environmental factors are temperature (constant or they go from dormancy (D) through conditional alternating), light:dark regime, and soil moisture. dormancy (CD: germinating over only a portion of Mean (± SE) optimum temperature for grass seeds the range of conditions possible for particular spe- requiring high summer temperature to break dor- cies) to non-dormancy (ND) (Baskin and Baskin mancy is 16.2 ± 1.1 °C for winter annuals, 27.2 ± 1998). Of the various types of dormancy exhibited 2.0 °C for perennials, and 29.9 ± 0.1 °C for summer 88 GRASSES AND GRASSLAND ECOLOGY annuals. For grass seeds requiring low winter tem- germination >50% down to –2.03 MPa. By contrast, peratures to come out of dormancy the optimum some grass seed (e.g. Zizania palustris, Spartina germination temperatures are 24.8 ± 1.1 °C for anglica —both wetland species) is recalcitrant, dying summer annuals and 23.5 ± 1.1 °C for perennials if its moisture content drops below 20–45%, and (Baskin and Baskin 1998). Some grass seeds require in others high moisture content experienced dur- alternating temperatures for germination (e.g. ing flooding prevents germination (e.g. Oryzopsis Agrostis capillaris, Dactylis glomerata, Lolium perenne). hymenoides, Blank and Young 1992). Water stress For some, alternating temperatures allow germi- interacts with temperature and light, controlling nation in darkness (e.g. Deschampsia caespitosa, Poa germination. For example, germination of Bromus pratensis). The germination response to alternating sterilis is inhibited by far-red (PFR) light, but only temperatures is viewed as a soil depth-detecting at temperatures <15 °C. Moreover, under low mois- mechanism and a canopy gap-detecting mecha- ture conditions, the inhibitory effect of PFR is nism (Thompson et al. 1977). This response occurs increased (Hilton 1984). Thus, light inhibition and because fluctuations in temperature decrease with moisture stress may delay germination of freshly increasing soil depth or increasing canopy cover. A shed seeds in the autumn, with low temperatures seed that germinates under alternating rather than and moisture stress preventing germination until constant temperature is thus more likely to be at a the following spring. shallow depth in the soil and/or under a canopy Other factors that affect germination include gap. In either case, germinating under these con- aspects of the soil chemical environment includ- – ditions will enhance the probability of survival of ing soil pH, minerals (especially NO3 ), salinity, the seedling. heavy metals, and organic compounds (Baskin The light:dark requirements for germination are and Baskin 1998; Fenner and Thompson 2005). Of controlled by the phytochrome system. Red (R) particular relevance in fire-prone grasslands is the light usually promotes germination, whereas far- promotion of seed germination by smoke. As a red (FR) light inhibits it. A low R:FR ratio is experi- germination cue, the effects of smoke vary among enced under light filtered through green canopies, species. In one study, percentage germination was and reduces the germination of some seeds (e.g. significantly increased in 8 of 20 species tested Apera spica-venti, Elymus repens, Lolium pratense, (Austrostipa scabra, Chloris ventricosa, Dichanthium Poa pratensis, Setaria verticillata) (Baskin and Baskin sericeum, Panicum decompositum, P. effusum, 1998), it may act to prevent germination of these Paspalidium distans, Poa labillardieri, and Themeda species under closed, shady grassland canopies. triandra) (Read and Bellairs 1999). In a similar Many grasses germinate better in light than in study, 16 of 22 species tested showed a significant the dark (e.g. Leptochloa filiformis, Muhlenbergia response to either smoke or heat (species showing schreberi), although some require darkness (e.g. a positive response to smoke were: Austrodanthonia Bromus sterilis). As with alternating temperatures, tenuior, Eragrostis benthamii, Entolasia leptostachya, the inhibition of germination under leaf canopies Panicum effusum, and P. simile (Clarke and French acts as a gap-detecting mechanism that has been 2005). These studies suggest that one way in which proposed to allow coexistence of species in grass- altered fire regimes change community structure lands. Experimental work in calcareous grasslands is through stimulation of different species through has supported this view (Silvertown 1980a). the effects of smoke and heat on germination. Soil moisture level is important for germination as the imbibition of water by the seed is the first Seedling establishment step towards germination. Water stress resulting Grass seedlings (see § 3.7) face multiple challenges from dry conditions reduces and inhibits germi- affecting survival and growth. As a result, mortal- nation of grasses. The mean ± SE soil moisture ity is usually high, reflecting the small size, soft stress reducing germination from 80–100% to palatable tissues, and limited reserves. Mortality 50% in grasses is –0.78 ± 0.09 MPa, with arid land may result from one of many factors, both abiotic grasses such as Bouteloua eriopoda able to maintain (burial, low light, flooding, drought, fire) and biotic POPULATION ECOLOGY 89
(predation, fungal, bacterial and viral disease, the older, ‘classic’ work on North American prai- mycorrhizae, intra- and interspecific competition) ries provides detailed descriptions of seedlings (Kitajima and Fenner 2000) (Table 5.1). For example, and the phenology of seedling establishment mortality of 24 seedling cohorts of Bromus tectorum while also noting the low density of seedlings observed over a 3 year period was principally due (Weaver and Fitzpatrick 1932). Even when seeds to desiccation in the first few months after emer- were artificially sown, seedling density was low gence (Fig. 5.2) (Mack and Pyke 1984). However, at and mortality very high due to summer drought, other times in the season, mortality due to disease winter frost, or insect herbivory (Blake 1935). More (smut Ustillago bullata), frost-heaving, and herbivory recent work has confirmed seedling regeneration by voles became important, varying in magnitude of the dominant species to be a rare and localized among sites. event in undisturbed prairie (Benson et al. 2004). The importance of seedling establishment as Significant numbers of seedlings emerge and a regenerative process in grasslands is variable, become established only when openings are cre- depending upon the system. Seedling regeneration ated or maintained, and then in moist years (Blake can be important following large-scale disturbance 1935; Glenn-Lewin et al. 1990). such as drought or fire (Glenn-Lewin et al. 1990) and Seedlings require a ‘safe site’ (Harper 1977) that locally on small-scale disturbances such as animal is often different in microhabitat characteristics burrow systems (Rabinowitz and Rapp 1985; Rapp from that of the adult plant. Appropriate safe sites and Rabinowitz 1985; Rogers and Hartnett 2001a) for seedlings are often rare in grasslands because (see Chapter 9). Catastrophic disturbances such of the competitiveness of the existing sward as the Great Drought of 1934 in the US Midwest (Defossé et al. 1997b). Many studies have char- killed many prairie dominants, allowing extensive acterized the safe sites or microsites suitable for seedling recruitment of drought-resistant species seedling establishment in grasslands and these such as Pascopyrum smithii and ruderals includ- generally involve a temporal or spatial release from ing the grass Bromus secalinus and forbs Conyza competition for resources such as light, moisture, canadensis, Lepidium virginicum, and Tragopogon and nutrients (Bisigato and Bertiller 2004; Defossé lamottei (Weaver and Albertson 1936). The impor- et al. 1997b; Dickinson and Dodd 1976; Romo 2005) tance of seedling regeneration in closed, mature, or herbivory (Edwards and Crawley 1999). As undisturbed grasslands is less certain. Much of noted already for North American prairies, gaps
Table 5.1 Fine-scale, primary factors and associated larger-scale environmental determinants affecting seedling establishment of grasses
Primary factors Primary determinants
Abiotic factors Local edaphic conditions (moisture, nutrients, aeration, etc.) Rainfall patterns and distribution; topography; soil type Light Daylength; vegetation structure/type; disturbance levels Temperature Regional climate; vegetation structure/type Biotic factors Competition Population density; vegetation structure/type; disturbance levels Neighbours (e.g., allelopathy, nurse plant effects) Population density; vegetation structure/type Herbivory Insect/mammal abundance; structural and chemical defences Litter Vegetation structure/type; decomposition rates; fire frequency Pathogens/mutualist/other symbionts Structural and chemical defences; environmental conditions (moisture, temperature, etc.); availability of inocula Maternal effects (e.g. seed size heteromorphism) Environmental conditions present during seed maturation; position of seed maturation on maternal plant
With permission from Cheplick (1998b). 90 GRASSES AND GRASSLAND ECOLOGY
Moist site Mesic site Dry site 40 81 85 1977–78 1977–78 1977–78
50 40 20 25 20
0 0 0
1978–79 380 730 1978–79 650 1978–79 670 320 400 451 260 180 180 200 120 120 60 60 Number of individuals 0 0 0
83 198 138 1979–80 1979–80 1979–80 142 60 40 40 40
20 20 20
0 0 0 S O N D J F M A M J J S O N D J F M A M J J S O N D J F M A M J Time (calendar month)
Figure 5.2 Mortality of Bromus tectorum seedlings from late summer 1977–June 1980 at three sites in eastern Washington, USA. ([dark grey], desiccation; ([hatched]), smut; ([black]), grazing; ([white]) winter death; ([light grey]), unknown. Reproduced with permission from Mack and Pyke (1984).
can provide the opportunity for seedling regen- describe successful seedling establishment in spe- eration. The size, duration, timing of gap forma- cific circumstances: tion, and interactions with other environmental factors such as grazers (Defossé et al. 1997a), all ● seasonal regeneration (S): independent off- interact to affect seedling regeneration success in spring (seeds or vegetative propagules) produced gaps (Bullock et al. 1995). In addition, the prop- in a single cohort ● agule rain may limit recruitment into safe sites persistent seed or spore bank (Bs): viable but (e.g. Edwards and Crawley 1999; Foster et al. 2004). dormant seeds or spores present throughout the As noted by Rapp and Rabinowitz (1985) studying year, some persisting >12 months seedling regeneration on to small-scale distur- ● numerous widely dispersed seeds or spores bances in prairies, seedling regeneration is indi- (W): offspring numerous and exceedingly buoy- vidualistic with establishment patterns differing ant in air; widely dispersed and often of limited among species. Badger disturbances in tallgrass persistence ● prairie, for example, have been shown to provide persistent juveniles (Bsd): offspring derived from sites for the establishment of distinct suites of an independent propagule but seedling or spore- ‘fugitive’ species unable to establish in otherwise ling capable of long-term persistence in a juvenile undisturbed prairie (Platt 1975). state Grime and Hillier (2000) recognize five regen- ● vegetative expansion (V): new vegetative shoots erative strategies for plants, of which the first four attached to parent plant at least until established. POPULATION ECOLOGY 91
It is argued by Grime and Hillier (2000) that the 5.1.5 Population dynamics importance of the five regeneration strategies will Births, deaths, immigration, and emigration regu- vary among different types of habitat, for example late density in a population (Harper 1977). While with W (production of numerous widely dispersed the total number of individuals may remain fairly seeds or spores) being the predominant regenera- constant in a population, there is considerable flux tive strategy in early successional habitats whereas in the number of individuals (Fig. 5.3). Here the persistent seed banks (B ) were predicted to be s implications for studying growth in grass popula- more important following disturbance in coppice tions are discussed. and heathland habitats. These ideas were tested Understanding population change can be for the three seed regenerative strategies (S, B , and s accomplished using recruitment curves and cal- W) in habitats around Derbyshire, UK (Table 5.2). culating population growth rate. A recruitment Of interest is the important role of both seasonal curve represents a plot of population size (N) at regeneration and the persistent seed bank (B ) in s the next census in the future (i.e. N ) against cur- the grasslands compared with early succession t+1 rent population size (N ) for populations governed habitats where regenerative strategy (W) is more t by density-dependent mortality (Silvertown and important and wooded habitats where seasonal Charlesworth 2001). Any population falling on the regeneration (S) is more important. Other inves- diagonal represented by N = N is at equilibrium. tigators have taken a different approach to clas- t+1 t The slope of the recruitment curve (N /N ) gives sifying regeneration strategies in grasslands. For t+1 t the value for lambda (λ), the annual (finite) rate example, seed size appears to be a relevant life- of population increase. For example, Watkinson history trait important in understanding the regen- (1990) conducted a 9 year study of the annual grass eration strategy of species in British calcareous Vulpia fasciculata in two dune systems in North grassland (Silvertown 1981) with large-seeded spe- Wales. Over that time, the density of V. fasciculata cies (1.0–3.0 mg) germinating in the spring when declined. Recruitment curves indicated a negative competition from established species for water and density-dependent relationship between fecun- nutrients is high. By contrast, small-seeded species dity and density consistent through time, despite (0.01–1.0 mg) germinate in the autumn when com- declining overall population density. Finite popu- petition is less. lation growth rates calculated from population estimates in consecutive years indicated a strong positive relationship with percentage cover of bare sand (Fig. 5.4a), which was used to calculate equi- Table 5.2 Relative importance (%) of the regenerative strategies, librium population size expected at various levels
S (Seasonal regeneration), Bs (Persistent seed or spore bank), and of sand cover (Fig. 5.4b). Populations of V. fasiculata W (Numerous dispersed seeds or spores) in established vegetation could only be expected to persist where bare sand of neighbouring habitats in Lathkill Dale, Derbyshire, UK exceeded 50%. A similar study on the annual grass Sorghum intrans again showed a negative density- Habitat S Bs W dependent relationship with fecundity mediated Cliffs 38 30 18 by environmental factors (Watkinson et al. 1989). Quarry heaps 44 40 18 For example, in local areas of poor growth poten- Calcareous grassland 50 45 5 tial, fecundity was too low to sustain the popula- Acid grassland 49 51 4 tions in the absence of immigration of seed from Unmanaged calcareous grassland 63 31 0 outside areas; a rescue effect (sensu Hanski and Scrub 52 21 1 Gyllenberg 1993). Deciduous woodland 73 30 1 The age- or stage-structure of a population and Note: percentages do not sum to 100 because the three categories are the probability of individuals in a population chang- not mutually exclusive, and some species could not be classified. ing over time to a different age- or stage state/class From Grime and Hillier (2000). (e.g. from a 1 year old plant to a 2 year old plant, 92 GRASSES AND GRASSLAND ECOLOGY
300 Cumulative births
200
100 Live tiller numbers
0
Number of tillers –100
–200 Cumulative deaths
–300 AM J J A SOONNDDMAM JJ A S F M A Month
Figure 5.3 Population flux in Lolium perenne (number of tillers). Reproduced with permission from Silvertown and Charlesworth (2001).
(a) (b) 104
2 103
102 [log ( n +l)]
1 –2 m 10 Number of flowering plants Finite rate of population increase 0 1 02040 60 80 100 020406080 Percentage cover of sand
Figure 5.4 The relationship between (a) the finite rate of population increase of Vulpia fasciculata and sand cover at two dune systems in North Wales, UK (open and closed symbols) (fitted regression, r2 = 0.40, p < 0.001), and (b) estimated equilibrium population density of V. fasciculata and sand cover. Reproduced with permission from Watkinson (1990). or from a seedling to a vegetative tussock, respec- of models have proved useful in understanding tively: see Fig. 3.4) can be incorporated into a pro- the population dynamics of important grassland jection (transition) matrix (Gibson 2002). From this species in response to environmental factors (e.g. matrix, λ can be estimated by comparing the ratio O’Connor 1994) and in allowing the development of the numbers in any one age/size class with the of best management practices to control the spread numbers in that class at the previous time interval. of invasive grassland weeds (Magda et al. 2004). An exact estimate for λ can be calculated at equilib- The contribution of different parts of the plants λ rium when a stable state structure is reached as the life cycle to can be calculated as elasticity (eij) dominant eigenvalue of the matrix. These types the proportion of λ due to an individual age/stage POPULATION ECOLOGY 93
transition (de Kroon et al. 1986). Thus, elasticity in moister years fecundity became more important provides a relative measure of a matrix element’s (Vega and Montaña 2004). Fire regime in grasslands λ contribution to fitness. Matrix model studies of this affects , which in Andropogon semiberbis in tropical type show that population growth in grasses can be savannah was in turn predominately affected by sensitive to particular age or stage states depending small size-class transitions, more so in the absence on the species and environmental setting (O’Connor of fire (61% elasticity) than under burned conditions 1993). Year-to-year variation in transitions can mark- (50%) (Silva et al. 1991). However, because in reality edly affect long-term population growth rates. For all these coefficients combine at least two different example, in Danthonia sericea temporal variability demographic processes or vital rates (e.g. stasis and affected recruitment of individuals from small into growth), one should calculate the elasticity of the large size classes, with the demographic success of vital rates implicit in each matrix coefficient (Franco the latter significantly affecting λ (Moloney 1986). and Silvertown 2004). A comparison of perennial Elasticity matrices can be decomposed to compare grasses on this basis shows the importance of these λ matrix coefficients that are dominated by different elasticities affecting (Table 5.3). Stasis (S) domi- demographic processes, i.e. S (stasis, staying in the nates these comparisons because of the importance same age or stage class from one transition period of the longevity of the clumps of these grasses com- to the next), G (growth, transitions to larger size- pared with growth (G). The contribution of the vital λ classes), and F (fecundity, reproduction via seed) rates reflecting fecundity (F) to was minor. (Silvertown et al. 1993). For example, in a comparison The contribution of life-cycle stages to popu- of six African savannah grasses, high population lation growth rates in annual grasses is poorly growth rates were frequently associated with sta- known. However, studies of other annuals sug- sis or growth (O’Connor 1994). The most important gest an important role for longevity of seed in contributions to population growth rates, however, the seed bank, the transition of individuals from generally involved the smallest size classes. seed to adult plants (Kalisz and McPeek 1992), Environmental variability greatly affects the driv- and fecundity (Fone 1989). Seed survival through ers of population growth, for example in dry years the winter, fecundity, and the proportion of seeds λ λ in Hilaria mutica, a semi-arid tussock grass, was escaping predation were important drivers of most affected by stasis and retrogression, whereas in agricultural populations of the annual grass
Table 5.3 Life-history characteristics of some perennial grasses: fi nite rate of population increase (λ), lifespan (L: expected age at death), age at sexual maturity (α: average age at which an individual enters a stage class
with positive fecundity), net reproductive rate (R0: average number of offspring produced by an individual over its life span), generation time (µ: mean age at which members of a cohort produce offspring), and elasticities (G: growth, F: fecundity, and S: stasis)