ecology of phytoplankton 2006

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Ecology of Phytoplankton

Phytoplankton communities dominate the pelagic

ecosystems that cover 70% of the world’s surface

area. In this marvellous new book Colin Reynolds

deals with the adaptations, physiology and popula-

tion dynamics of the phytoplankton communities

of lakes and rivers, of seas and the great oceans.

The book will serve both as a text and a major

work of reference, providing basic information on

composition, morphology and physiology of themain phyletic groups represented in marine and

freshwater systems. In addition Reynolds reviews

recent advances in community ecology, developing

an appreciation of assembly processes, coexistence

and competition, disturbance and diversity. Aimed

primarily at students of the plankton, it develops

many concepts relevant to ecology in the widest

sense, and as such will appeal to a wide readership

among students of ecology, limnology and oceanog-

raphy.

Born in London, Colin completed his formal edu-

cation at Sir John Cass College, University of Lon-

don. He worked briefly with the Metropolitan Water

Board and as a tutor with the Field Studies Coun-

cil. In 1970, he joined the staff at the Windermere

Laboratory of the Freshwater Biological Association.

He studied the phytoplankton of eutrophic meres,

then on the renowned ‘Lund Tubes’, the large lim-

netic enclosures in Blelham Tarn, before turning his

attention to the phytoplankton of rivers. During the

1990s, working with Dr Tony Irish and, later, also Dr

Alex Elliott, he helped to develop a family of models based on, the dynamic responses of phytoplankton

populations that are now widely used by managers.

He has published two books, edited a dozen others

and has published over 220 scientific papers as

well as about 150 reports for clients. He has

given advanced courses in UK, Germany, Argentina,

Australia and Uruguay. He was the winner of the

1994 Limnetic Ecology Prize; he was awarded a cov-

eted Naumann–Thienemann Medal of SIL and was

honoured by Her Majesty the Queen as a Member of

the British Empire. Colin also served on his munici-

pal authority for 18 years and was elected mayor of

Kendal in 1992–93.


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e c o l o g y , b i o d i v e r s i t y , a n d c o n s e r v a t i o n

Series editors

Michael Usher University of Stirling, and formerly Scottish Natural Heritage

Denis Saunders Formerly CSIRO Division of Sustainable Ecosystems, CanberraRobert Peet University of North Carolina, Chapel Hill

Andrew Dobson Princeton University

Editorial Board

Paul Adam University of New South Wales, Australia

H. J. B. Birks University of Bergen, Norway

Lena Gustafsson Swedish University of Agricultural Science

Jeff McNeely International Union for the Conservation of Nature

R. T. Paine University of Washington

David Richardson University of Cape Town

Jeremy Wilson Royal Society for the Protection of Birds

The world’s biological diversity faces unprecedented threats. The urgent challenge facing the con-

cerned biologist is to understand ecological processes well enough to maintain their functioning in

the face of the pressures resulting from human population growth. Those concerned with the con-

servation of biodiversity and with restoration also need to be acquainted with the political, social,

historical, economic and legal frameworks within which ecological and conservation practice must

be developed. This series will present balanced, comprehensive, up-to-date and critical reviews of

selected topics within the sciences of ecology and conservation biology, both botanical and zoo-

logical, and both ‘pure’ and ‘applied’. It is aimed at advanced (final-year undergraduates, graduate

students, researchers and university teachers, as well as ecologists and conservationists in indus-try, government and the voluntary sectors. The series encompasses a wide range of approaches and

scales (spatial, temporal, and taxonomic), including quantitative, theoretical, population, community,

ecosystem, landscape, historical, experimental, behavioural and evolutionary studies. The emphasis

is on science related to the real world of plants and animals, rather than on purely theoretical

abstractions and mathematical models. Books in this series will, wherever possible, consider issues

from a broad perspective. Some books will challenge existing paradigms and present new ecological

concepts, empirical or theoretical models, and testable hypotheses. Other books will explore new

approaches and present syntheses on topics of ecological importance.

Ecology and Control of Introduced Plants Judith H. Myers and Dawn R. Bazely

Invertebrate Conservation and Agricultural Ecosystems T. R. New

Risks and Decisions for Conservation and Environmental Management Mark Burgman

Nonequilibrium Ecology Klaus Rohde

Ecology of Populations Esa Ranta, Veijo Kaitala and Per Lundberg


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The Ecology of PhytoplanktonC. S. Reynolds


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Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo

Cambridge University PressThe Edinburgh Building, Cambridge , UK

First published in print format

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© Cambridge University Press 2006

2006

Information on this title: www.cambridge.org/9780521844130

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

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Cambridge University Press has no responsibility for the persistence or accuracy of sfor external or third-party internet websites referred to in this publication, and does notguarantee that any content on such websites is, or will remain, accurate or appropriate.

Published in the United States of America by Cambridge University Press, New York

www.cambridge.org

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This book is dedicated to

my wife, JEAN, to whom its writing

represented an intrusion into

domestic life, and to Charles Sinker,

John Lund and Ramón Margalef. Each is

a constant source of inspiration to me.


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Contents

Preface page ix

Acknowledgements xii

Chapter 1. Phytoplankton 11.1 Definitions and terminology 1

1.2 Historical context of phytoplankton studies 3

1.3 The diversification of phytoplankton 4

1.4 General features of phytoplankton 15

1.5 The construction and composition of freshwater

phytoplankton 24

1.6 Marine phytoplankton 34

1.7 Summary 36

Chapter 2. Entrainment and distribution in the pelagic 382.1 Introduction 38

2.2 Motion in aquatic environments 39

2.3 Turbulence 42

2.4 Phytoplankton sinking and floating 49

2.5 Adaptive and evolutionary mechanisms for

regulating ws 53

2.6 Sinking and entrainment in natural turbulence 67

2.7 The spatial distribution of phytoplankton 77

2.8 Summary 90

Chapter 3. Photosynthesis and carbon acquisition inphytoplankton 933.1 Introduction 93

3.2 Essential biochemistry of photosynthesis 94

3.3 Light-dependent environmental sensitivity of

photosynthesis 101

3.4 Sensitivity of aquatic photosynthesis to carbon

sources 124

3.5 Capacity, achievement and fate of primary

production at the ecosystem scale 1313.6 Summary 143

Chapter 4. Nutrient uptake and assimilation inphytoplankton 1454.1 Introduction 145

4.2 Cell uptake and intracellular transport of

nutrients 146

4.3 Phosphorus: requirements, uptake, deployment in

phytoplankton 151


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viii CONTENTS

4.4 Nitrogen: requirements, sources, uptake and

metabolism in phytoplankton 161

4.5 The role of micronutrients 166

4.6 Major ions 171

4.7 Silicon: requirements, uptake, deployment in

phytoplankton 173

4.8 Summary 175

Chapter 5. Growth and replication of phytoplankton 1785.1 Introduction: characterising growth 178

5.2 The mechanics and control of growth 179

5.3 The dynamics of phytoplankton growth and

replication in controlled conditions 183

5.4 Replication rates under sub-ideal conditions 189

5.5 Growth of phytoplankton in natural

environments 217

5.6 Summary 236

Chapter 6. Mortality and loss processes in phytoplankton 2396.1 Introduction 239

6.2 Wash-out and dilution 240

6.3 Sedimentation 243

6.4 Consumption by herbivores 250

6.5 Susceptibility to pathogens and parasites 292

6.6 Death and decomposition 296

6.7 Aggregated impacts of loss processes on

phytoplankton composition 297

6.8 Summary 300

Chapter 7. Community assembly in the plankton: pattern,process and dynamics 3027.1 Introduction 302

7.2 Patterns of species composition and temporal

change in phytoplankton assemblages 302

7.3 Assembly processes in the phytoplankton 350

7.4 Summary 385

Chapter 8. Phytoplankton ecology and aquatic ecosystems:mechanisms and management 3878.1 Introduction 387

8.2 Material transfers and energy flow in pelagic

systems 387

8.3 Anthropogenic change in pelagic environments 395

8.4 Summary 432

8.5 A last word 435

Glossary 437

Units, symbols and abbreviations 440


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CONTENTS

References 447

Index to lakes, rivers and seas 508

Index to genera and species of

phytoplankton 511

Index to genera and species of other

organisms 520

General index 524


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Preface

This is the third book I have written on the sub-

ject of phytoplankton ecology. When I finished

the first, The Ecology of Freshwater Phytoplankton(Reynolds, 1984a), I vowed that it would also be

my last. I felt better about it once it was pub-

lished but, as I recognised that science was mov-

ing on, I became increasingly frustrated about

the growing datedness of its information. When

an opportunity was presented to me, in the form

of the 1994 Ecology Institute Prize, to write my

second book on the ecology of plankton, Vege-

tation Processes in the Pelagic (Reynolds, 1997a), I

was able to draw on the enormous strides that

were being made towards understanding the part

played by the biochemistry, physiology and pop-

ulation dynamics of plankton in the overall func-

tioning of the great aquatic ecosystems. Any feel-

ing of satisfaction that that exercise brought to

me has also been overtaken by events of the last

decade, which have seen new tools deployed to

the greater amplification of knowledge and new

facts uncovered to be threaded into the web of

understanding of how the world works.

Of course, this is the way of science. Thereis no scientific text that can be closed with a

sigh, ‘So that’s it, then’. There are always more

questions. I actually have rather more now than

I had at the same stage of finishing the 1984 vol-

ume. No, the best that can be expected, or even

hoped for, is a periodic stocktake: ‘This is what

we have learned, this is how we think we can

explain things and this is where it fits into what

we thought we knew already; this will stand until

we learn something else.’ This is truly the way

of science. Taking observations, verifying them by experimentation, moving from hypothesis to

fact, we are able to formulate progressively closer

approximations to the truth.

In fact, the second violation of my 1984 vow

has a more powerful and less high-principled

driver. It is just that the progress in plankton

ecology since 1984 has been astounding, turning

almost each one of the first book’s basic assump-

tions on its head. Besides widening the scope of

the present volume to address more overtly the

marine phytoplankton, I have set out to construct

a new perspective on the expanded knowledge base. I have to say at once that the omission of

‘freshwater’ from the new title does not imply

that the book covers the ecology of marine plank-

ton in equivalent detail. It does, however, signify

a genuine attempt to bridge the deep but wholly

artificial chasm that exists between marine and

freshwater science, which political organisation

and science funding have perpetuated.

At a personal level, this wider view is a satisfy-

ing thing to develop, being almost a plea for abso-

lution – ‘I am sorry for getting it wrong before,

this is what I should have said!’ At a wider level, I

am conscious that many people still use and fre-

quently cite my 1984 book; I would like them to

know that I no longer believe everything, or even

very much, of what I wrote then. As if to empha-

sise this, I have adopted a very similar approach

to the subject, again using eight chapters (albeit

with altered titles). These are developed accord-

ing to a similar sequence of topics, through mor-

phology, suspension, ecophysiology and dynam-ics to the structuring of communities and their

functions within ecosystems. This arrangement

allows me to contrast directly the new knowl-

edge and the understanding it has rendered

redundant.

So just what are these mould-breaking

findings? In truth, they impinge upon the sub-

ject matter in each of the chapters. Advances in

microscopy have allowed ultrastructural details

of planktic organisms to be revealed for the first

time. The advances in molecular biology, in par-ticular the introduction of techniques for iso-

lating chromosomes and ribosomes, fragmenting

them by restriction enzymes and reading genetic

sequences, have totally altered perceptions about

phyletic relationships among planktic taxa and

suppositions about their evolution. The classifica-

tion of organisms is undergoing change of revolu-

tionary proportions, while morphological varia-

tion among (supposedly) homogeneous genotypes


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xii PREFACE

questions the very concept of putting names

to individual organisms. At the scale of cells,

the whole concept of how they are moved in

the water has been addressed mathematically.

It is now appreciated that planktic cells experi-

ence critical physical forces that are very differ-

ent from those affecting (say) fish: viscosity andsmall-scale turbulence determine the immediate

environment of microorganisms; surface tension

is a lethal and inescapable spectre; while shear

forces dominate dispersion and the spatial dis-

tributions of populations. These discoveries flow

from the giant leaps in quantification and mea-

surements made by physical limnologists and

oceanographers since the early 1980s. These have

also impinged on the revision of how sinking

and settlement of phytoplankton are viewed and

they have helped to consolidate a robust theory

of filter-feeding by zooplankton.

The way in which nutrients are sequestered

from dilute and dispersed sources in the water

and then deployed in the assembly and replica-

tion of new generations of phytoplankton has

been intensively investigated by physiologists.

Recent findings have greatly modified percep-

tions about what is meant by ‘limiting nutrients’

and what happens when one or other is in short

supply. As Sommer (1996) commented, past sup-

positions about the repercussions on community

structure have had to be revised, both through

the direct implications for interspecific compe-

tition for resources and, indirectly, through the

effects of variable nutritional value of potential

foods to the web of dependent consumers.

Arguably, the greatest shift in understanding

concerns the way in which the pelagic ecosys-

tem works. Although the abundance of plank-

tic bacteria and the relatively vast reserve of

dissolved organic carbon (DOC) had long beenrecognised, the microorganismic turnover of car-

bon has only been investigated intensively dur-

ing the last two decades. It was soon recog-

nised that the metazoan food web of the open

oceans is linked to the producer network via

the turnover of the microbes and that this state-

ment applies to many larger freshwater systems

as well. The metabolism of the variety of sub-

stances embraced by ‘DOC’ varies with source and

chain length but a labile fraction originates from

phytoplankton photosynthesis that is leaked or

actively discharged into the water. Far from hold-

ing to the traditional view of the pelagic food

chain – algae, zooplankton, fish – plankton ecol-

ogists now have to acknowledge that marine

food webs are regulated ‘by a sea of microbes’

(Karl, 1999), through the muliple interactions of organic and inorganic resources and by the lock

of protistan predators and acellular pathogens

(Smetacek, 2002). Even in lakes, where the case

for the top–down control of phytoplankton by

herbivorous grazers is championed, the other-

wise dominant microbially mediated supply of

resources to higher trophic levels is demonstra-

bly subsidised by components from the littoral

(Schindler et al., 1996; Vadeboncoeur et al., 2002).

There have been many other revolutions. One

more to mention here is the progress in ecosys-

tem ecology, or more particularly, the bridge

between the organismic and population ecology

and the behaviour of entire systems. How ecosys-

tems behave, how their structure is maintained

and what is critical to that maintenance, what

the biogeochemical consequences might be and

how they respond to human exploitation and

management, have all become quantifiable. The

linking threads are based upon thermodynamic

rules of energy capture, exergy storage and struc-

tural emergence, applied through to the systems

level (Link, 2002; Odum, 2002).

In the later chapters in this volume, I attempt

to apply these concepts to phytoplankton-based

systems, where the opportunity is again taken

to emphasise the value to the science of ecol-

ogy of studying the dynamics of microorganisms

in the pursuit of high-order pattern and assem-

bly rules (Reynolds, 1997, 2002b). The dual chal-

lenge remains, to convince students of forests

and other terrestrial ecosystems that microbialsystems do conform to analogous rules, albeit

at very truncated real-time scales, and to per-

suade microbiologists to look up from the micro-

scope for long enough to see how their knowl-

edge might be applied to ecological issues.

I am proud to acknowledge the many people

who have influenced or contributed to the sub-

ject matter of this book. I thank Charles Sinker

for inspiring a deep appreciation of ecology and

its mechanisms. I am grateful to John Lund, CBE,


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PREFACE x

FRS for the opportunity to work on phytoplank-

ton as a postgraduate and for the constant inspi-

ration and access to his knowledge that he has

given me. Of the many practising theoretical ecol-

ogists whose works I have read, I have felt the

greatest affinity to the ideas and logic of Ramón

Margalef; I greatly enjoyed the opportunities todiscuss these with him and regret that there will

be no more of them.

I gratefully acknowledge the various scien-

tists whose work has profoundly influenced par-

ticular parts of this book and my thinking gen-

erally. They include (in alphabetical order) Sal-

lie Chisholm, Paul Falkowski, Maciej Gliwicz,

Phil Grime, Alan Hildrew, G. E. Hutchinson, Jörg

Imberger, Petur Jónasson, Sven-Erik Jørgensen,

Dave Karl, Winfried Lampert, John Lawton, John

Raven, Marten Scheffer, Ted Smayda, Milan

Straškraba, Reinhold T ̈uxen, Anthony Walsby and

Thomas Weisse. I have also been most fortu-

nate in having been able, at various times, to

work with and discuss many ideas with col-

leagues who include Keith Beven, Sylvia Bonilla,

Odécio Cáceres, Paul Carling, Jean-Pierre Descy,

Mónica Diaz, Graham Harris, Vera Huszar, Dieter

Imboden, Kana Ishikawa, Medina Kadiri, Susan

Kilham, Michio Kumagai, Bill Li, Vivian Monte-

cino, Mohi Munawar, Masami Nakanishi, Shin-

Ichi Nakano, Luigi Naselli-Flores, Pat Neale, Søren

Nielsen, Judit Padisák, Fernando Pedrozo, Victor

Smetaček, Ulrich Sommer, José Tundisi and

Peter Tyler. I am especially grateful to Cather-

ine Legrand who generously allowed me to use

and interpret her experimental data on Alexan-

drium. Nearer to home, I have similarly benefited

from long and helpful discussions with such erst-

while Windermere colleagues as Hilda Canter-

Lund, Bill Davison, Malcolm Elliott, Bland Finlay,

Glen George, Ivan Heaney, Stephen Maberly, Jack Talling and Ed Tipping.

During my years at The Ferry House, I was

ably and closely supported by several co-workers,

among whom special thanks are due to Tony

Irish, Sheila Wiseman, George Jaworski and Brian

Godfrey. Peter Allen, Christine Butterwick, Julie

Corry (later Parker), Mitzi De Ville, Joy Elsworth,

Alastair Ferguson, Mark Glaister, David Gouldney,

Matthew Rogers, Stephen Thackeray and Julie

Thompson also worked with me at particulartimes. Throughout this period, I was privileged

to work in a ‘well-found’ laboratory with abun-

dant technical and practical support. I freely

acknowledge use of the world’s finest collection

of the freshwater literature and the assistance

provided at various times by John Horne, Ian

Pettman, Ian McCullough, Olive Jolly and Mari-

lyn Moore. Secretarial assistance has come from

Margaret Thompson, Elisabeth Evans and Joyce

Hawksworth. Trevor Furnass has provided abun-

dant reprographic assistance over many years. I

am forever in the debt of Hilda Canter-Lund, FRPS

for the use of her internationally renowned pho-

tomicrographs.

A special word is due to the doctoral students

whom I have supervised. The thirst for knowl-

edge and understanding of a good pupil gener-

ally provide a foil and focus in the other direc-

tion. I owe much to the diligent curiosity of Chris

van Vlymen, Helena Cmiech, Karen Saxby (now

Rouen), Siân Davies, Alex Elliott, Carla Kruk and

Phil Davis.

My final word of appreciation is reserved for

acknowledgement of the tolerance and forbear-

ance of my wife and family. I cheered through

many juvenile football matches and dutifully

attended a host of ballet and choir performances

and, yes, it was quite fun to relive three more

school curricula. Nevertheless, my children had

less of my time than they were entitled to expect.

Jean has generously shared with my science the

full focus of my attention. Yet, in 35 years of mar-riage, she has never once complained, nor done

less than encourage the pursuit of my work. I am

proud to dedicate this book to her.


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Acknowledgements

Except where stated, the illustrations in this book

are reproduced, redrawn or otherwise slightly

modified from sources noted in the individualcaptions. The author and the publisher are grate-

ful to the various copyright holders, listed below,

who have given permission to use copyright mate-

rial in this volume. While every effort has been

made to clear permissions as appropriate, the

publisher would appreciate notification of any

omission.

Figures 1.1 to 1.8, 1.10, 2.8 to 2.13, 2.17, 2.20 to

2.31, 3.3 to 3.9, 3.16 and 3.17, 5.20, 6.2, 6.7, 6.11.

7.6 and 7.18 are already copyrighted to CambridgeUniversity Press.

Figure 1.9 is redrawn by permission of Oxford

University Press.

Figure 1.11 is the copyright of the American Soci-

ety of Limnology and Oceanography.

Figures 2.1 and 2.2, 2.5 to 2.7, 2.15 and 2.16, 2.18

and 2.19, 3.12, 3.14, 3.19, 4.1, 4.3 to 4.5, 5.1 to

5.5, 5.8, 5.10, 5.12 and 5.13, 5.20 and 5.21, 6.1,

6.2, 6.4, 6.14, 7.8, 7.10 and 7.11, 7.14, 7.16 and 7.17,7.20 and 7.22 are redrawn by permission of The

Ecology Institute, Oldendorf.

Figures 2.3 and 4.7 are redrawn from the source

noted in the captions, with acknowledgement to

Artemis Press.

Figures 2.4, 3.18, 5.11, 5.18, 7.5, 7.15, 8.2 and 8.3

are redrawn from the various sources noted in

the respective captions and with acknowledge-

ment to Elsevier Science, B.V.

Figure 2.14 is redrawn from the British Phycologi-

cal Journal by permission of Taylor & Francis Ltd

(http://www.tandf.co.uk/journals).

Figure 3.1 is redrawn by permission of Nature

Publishing Group.

Figures 3.2, 3.11, 3.13, 4.2, 5.6, 6.4, 6.6, 6.9,

6.10 and 6.13 come from various titles that are

the copyright of Blackwell Science (the specific

sources are noted in the figure captions) and are

redrawn by permission.

Figures 3.7, 3.15, 4.6 and 7.2.3 (or parts thereof)

are redrawn from Freshwater Biology by permission

of Blackwell Science.

Figure 3.7 incorporates items redrawn from Bio-

logical Reviews with acknowledgement to the Cam-

bridge Philosophical Society.

Figure 5.9 is redrawn by permission of John Wiley

& Sons Ltd.

Figure 5.14 is redrawn by permission of Springer-

Verlag GmbH.

Figures 5.15 to 5.17, 5.19, 6.8 and 6.9 are redrawn

by permission of SpringerScience+Business BV.Figures 6.12, 6.15, 7.1 to 7.4, 7.9 and 8.6 are repro-

duced from Journal of Plankton Research by permis-

sion of Oxford University Press. Dr K. Bruning also

gave permission to produce Fig. 6.12.

Figure 7.7 is redrawn by permission of the Direc-

tor, Marine Biological Association.

Figures 7.12 to 7.14, 7.24 and 7.25 are redrawn

from Verhandlungen der internationale Vereini-

gung f ̈ur theoretische und angewandte Limnolo-

gie by permission of Dr E. Nägele (Publisher)

(http://www.schwezerbart.de).

Figure 7.19 is redrawn with acknowledgement to

the Athlone Press of the University of London.

Figure 7.21 is redrawn from Aquatic Ecosystems

Health and Management by permission of Taylor

& Francis, Inc. (http://www.taylorandfrancis.com).

Figure 8.1 is redrawn from Scientia Maritima by

permission of Institut de Ciències del Mar.

Figures 8.5, 8.7 and 8.8 are redrawn by permis-

sion of the Chief Executive, Freshwater Biological

Association.


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Chapter 1

Phytoplankton

1.1 Definitions and terminology

The correct place to begin any exposition of a

major component in biospheric functioning is

with precise definitions and crisp discrimination.

This should be a relatively simple exercise but for

the need to satisfy a consensus of understand-

ing and usage. Particularly among the biological

sciences, scientific knowledge is evolving rapidly

and, as it does so, it often modifies and outgrows

the constraints of the previously acceptable ter-

minology. I recognised this problem for plank-

ton science in an earlier monograph (Reynolds,

1984a). Since then, the difficulty has worsened

and it impinges on many sections of the present

book. The best means of dealing with it is to

accept the issue as a symptom of the good health

and dynamism of the science and to avoid con-

straining future philosophical development by a

redundant terminological framework.

The need for definitions is not subverted, how-

ever, but it transforms to an insistence that those

that are ventured are provisional and, thus, open

to challenge and change. To be able to revealsomething also of the historical context of the

usage is to give some indication of the limitations

of the terminology and of the areas of conjecture

impinging upon it.

So it is with ‘ plankton’. The general under-

standing of this term is that it refers to the col-

lective of organisms that are adapted to spend part

or all of their lives in apparent suspension in the

open water of the sea, of lakes, ponds and rivers.

The italicised words are crucial to the concept

and are not necessarily contested. Thus, ‘plank-

ton’ excludes other suspensoids that are either

non-living, such as clay particles and precipitated

chemicals, or are fragments or cadavers derived

from biogenic sources. Despite the existence of

the now largely redundant subdivision tychoplank-

ton (see Box 1.1), ‘plankton’ normally comprises

those living organisms that are only fortuitously

and temporarily present, imported from adjacent

habitats but which neither grew in this habitat

nor are suitably adapted to survive in the truly

open water, ostensibly independent of shore and

bottom. Such locations support distinct suites of

surface-adhering organisms with their own dis-

tinctive survival adaptations.

‘Suspension’ has been more problematic, hav-

ing quite rigid physical qualifications of dens-

ity and movement relative to water. As will be

rehearsed in Chapter 2, only rarely can plank-

ton be isopycnic (having the same density) with

the medium and will have a tendency to float

upwards or sink downwards relative to it. The

rate of movement is also size dependent, so

that ‘apparent suspension’ is most consistently

achieved by organisms of small (


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2 PHYTOPLANKTON

Box 1.1 Some definitions used in the literaureon plankton

seston the totality of particulate matter in water; all material not

in solution

tripton non-living seston

plankton living seston, adapted for a life spent wholly or partly in

quasi-suspension in open water, and whose powers of

motility do not exceed turbulent entrainment (see

Chapter 2)

nekton animals adapted to living all or part of their lives in open

water but whose intrinsic movements are almost

independent of turbulence

euplankton redundant term to distinguish fully adapted, truly planktic

organisms from other living organisms fortuitously

present in the water

tychoplankton non-adapted organisms from adjacent habitats and

present in the water mainly by chance

meroplankton planktic organisms passing a major part of the life history

out of the plankton (e.g. on the bottom sediments)

limnoplankton plankton of lakes

heleoplankton plankton of ponds

potamoplankton plankton of rivers

phytoplankton planktic photoautotrophs and major producer of the

pelagic

bacterioplankton planktic prokaryotes

mycoplankton planktic fungi

zooplankton planktic metazoa and heterotrophic protistans

Some more, now redundant, terms

The terms nannoplankton, ultraplankton, µ-algae are older names for various smaller

size categories of phytoplankton, eclipsed by the classification of Sieburth et al.

(1978) (see Box 1.2).

In this way, plankton comprises organisms

that range in size from that of viruses (a few tensof nanometres) to those of large jellyfish (a metre

or more). Representative organisms include bac-

teria, protistans, fungi and metazoans. In the

past, it has seemed relatively straightforward to

separate the organisms of the plankton, both

into broad phyletic categories (e.g. bacterioplank-

ton, mycoplankton) or into similarly broad func-

tional categories (photosynthetic algae of the

phytoplankton, phagotrophic animals of the zoo-

plankton). Again, as knowledge of the organ-

isms, their phyletic affinities and physiological

capabilities has expanded, it has become clearthat the divisions used hitherto do not pre-

cisely coincide: there are photosynthetic bac-

teria, phagotrophic algae and flagellates that take

up organic carbon from solution. Here, as in gen-

eral, precision will be considered relevant and

important in the context of organismic prop-

erties (their names, phylogenies, their morpho-

logical and physiological characteristics). On the

other hand, the generic contributions to sys-

tems (at the habitat or ecosystem scales) of the


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HISTORICAL CONTEXT OF PHYTOPLANKTON STUDIES

photosynthetic primary producers, phagotrophic

consumers and heterotrophic decomposers may

be attributed reasonably but imprecisely to phyto-

plankton, zooplankton and bacterioplankton.

The defintion of phytoplankton adopted for

this book is the collective of photosynthetic

microorganisms, adapted to live partly or contin-uously in open water. As such, it is the photoau-

totrophic part of the plankton and a major pri-

mary producer of organic carbon in the pelagic

of the seas and of inland waters. The distinction

of phytoplankton from other categories of plank-

ton and suspended matter are listed in Box 1.1.

It may be added that it is correct to refer to

phytoplankton as a singular term (‘ phytoplank-

ton is’ rather than ‘phytoplankton are’). A single

organism is a phytoplanktont or (more ususally)

phytoplankter . Incidentally, the adjective ‘plank-

tic’ is etymologically preferable to the more com-

monly used ‘planktonic’.

1.2 Historical context of phytoplankton studies

The first use of the term ‘plankton’ is attributed

in several texts (Ruttner, 1953; Hutchinson, 1967)

to Viktor Hensen, who, in the latter half of the

nineteenth century, began to apply quantitative

methods to gauge the distribution, abundance

and productivity of the microscopic organisms

of the open sea. The monograph that is usually

cited (Hensen, 1887) is, in fact, rather obscure

and probably not well read in recent times but

Smetacek et al. (2002) have provided a probing

and engaging review of the original, within the

context of early development of plankton science.

Most of the present section is based on theirarticle.

The existence of a planktic community of

organisms in open water had been demonstrated

many years previously by Johannes Müller. Knowl-

edge of some of the organisms themselves

stretches further back, to the earliest days

of microscopy. From the 1840s, Müller would

demonstrate net collections to his students, using

the word Auftrieb to characterise the commu-

nity (Smetacek et al., 2002). The literal transla-

tion to English is ‘up drive’, approximately ‘buoy-

ancy’ or ‘flotation’, a clear reference to Müller’s

assumption that the material floated up to the

surface waters – like so much oceanic dirt! It

took one of Müller’s students, Ernst Haeckel, to

champion the beauty of planktic protistans and

metazoans. His monograph on the Radiolaria was also one of the first to embrace Darwin’s

(1859) evolutionary theory in order to show

structural affinities and divergences. Haeckel, of

course, became best known for his work on

morphology, ontogeny and phylogeny. According

to Smetacek et al. (2002), his interest and skills

as a draughtsman advanced scientific awareness

of the range of planktic form (most significantly,

Haeckel, 1904) but to the detriment of any real

progress in understanding of functional differen-

tiation. Until the late 1880s, it was not appreci-

ated that the organisms of the Auftrieb, even the

algae among them, could contribute much to the

nutrition of the larger animals of the sea. Instead,

it seems to have been supposed that organic mat-

ter in the fluvial discharge from the land was the

major nutritive input. It is thus rather interest-

ing to note that, a century or so later, this pos-

sibility has enjoyed something of a revival (see

Chapters 3 and 8).

If Haeckel had conveyed the beauty of the

pelagic protistans, it was certainly Viktor Hensen

who had been more concerned about their role

in a functional ecosystem. Hensen was a phys-

iologist who brought a degree of empiricism

to his study of the perplexing fluctuations in

North Sea fish stocks. He had reasoned that

fish stocks and yields were related to the pro-

duction and distribution of the juvenile stages.

Through devising techniques for sampling, quan-

tification and assessing distribution patterns,

always carefully verified by microscopic exami-nation, Hensen recognised both the ubiquity of

phytoplankton and its superior abundance and

quality over coastal inputs of terrestrial detritus.

He saw the connection between phytoplankton

and the light in the near-surface layer, the nutri-

tive resource it provided to copepods and other

small animals, and the value of these as a food

source to fish.

Thus, in addition to bequeathing a new

name for the basal biotic component in pelagic


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4 PHYTOPLANKTON

ecosystems, Hensen may be regarded justifiably

as the first quantitative plankton ecologist and

as the person who established a formal method-

ology for its study. Deducing the relative contri-

butions of Hensen and Haeckel to the founda-

tion of modern plankton science, Smetacek et al.

(2002) concluded that it is the work of the lat-ter that has been the more influential. This is an

opinion with which not everyone will agree but

this is of little consequence. However, Smetacek

et al. (2002) offered a most profound and resonant

observation in suggesting that Hensen’s general

understanding of the role of plankton (‘the big

picture’) was essentially correct but erroneous in

its details, whereas in Haeckel’s case, it was the

other way round. Nevertheless, both have good

claim to fatherhood of plankton science!

1.3 The diversification of phytoplankton

Current estimates suggest that between 4000 and

5000 legitimate species of marine phytoplank-

ton have been described (Sournia et al. 1991;

Tett and Barton, 1995). I have not seen a com-

parable estimate for the number of species in

inland waters, beyond the extrapolation I made

(Reynolds, 1996a) that the number is unlikely to

be substantially smaller. In both lists, there is

not just a large number of mutually distinct taxa

of photosynthetic microorganisms but there is a

wide variety of shape, size and phylogenetic affin-

ity. As has also been pointed out before (Reynolds,

1994a), the morphological range is comparable to

the one spanning forest trees and the herbs that

grow at their base. The phyletic divergence of the

representatives is yet wider. It would be surpris-ing if the species of the phytoplankton were uni-

form in their requirements, dynamics and sus-

ceptibilities to loss processes. Once again, there

is a strong case for attempting to categorise the

phytoplankton both on the phylogeny of organ-

isms and on the functional basis of their roles in

aquatic ecosystems. Both objectives are adopted

for the writing of this volume. Whereas the for-

mer is addressed only in the present chapter, the

latter quest occupies most of the rest of the book.

However, it is not giving away too much to antici-

pate that systematics provides an important foun-

dation for species-specific physiology and which

is itself part-related to morphology. Accordingly,

great attention is paid here to the differentia-

tion of individualistic properties of representa-tive species of phytoplankton.

However, there is value in being able simul-

taneously to distinguish among functional cate-

gories (trees from herbs!). The scaling system and

nomenclature proposed by Sieburth et al. (1978)

has been widely adopted in phytoplankton ecol-

ogy to distinguish functional separations within

the phytoplankton. It has also eclipsed the use of

such terms as µ -algae and ultraplankton to separate

the lower size range of planktic organisms from

those (netplankton) large enough to be retained

by the meshes of a standard phytoplankton net.

The scheme of prefixes has been applied to size

categories of zooplankton, with equal success.

The size-based categories are set out in Box 1.2.

At the level of phyla, the classification of

the phytoplankton is based on long-standing cri-

teria, distinguished by microscopists and bio-

chemists over the last 150 years or so, from

which there is little dissent. In contrast, subdi-

vision within classes, orders etc., and the tracing

of intraphyletic relationships, affinities within

and among families, even the validity of suppos-

edly well-characterised species, has become sub-

ject to massive reappraisal. The new factor that

has come into play is the powerful armoury of

the molecular biologists, including the methods

for reading gene sequences and for the statisti-

cal matching of these to measure the closeness

to other species.

Of course, the potential outcome is a much

more robust, genetically verified family tree of authentic species of phytoplankton. This may be

some years away. For the present, it seems point-

less to reproduce a detailed classification of the

phytoplankton that will soon be made redun-

dant. Even the evolutionary connectivities among

the phyla and their relationship to the geochem-

ical development of the planetary structures

are undergoing deep re-evaluation (Delwiche,

2000; Falkowski, 2002). For these reasons, the


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THE DIVERSIFICATION OF PHYTOPLANKTON

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

Maximum linear dimension Namea

0.2–2 µ m picophytoplankton

2–20 µ m nanophytoplankton

20–200 µ m microphytoplankton

200 µ m–2 mm mesophytoplankton

>2 mm macrophytoplankton

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

‘flagellates’, etc.

taxonomic listings in Table 1.1 are deliberately

conservative.

Although the life forms of the plankton

include acellular microorganisms (viruses) and a

range of well-characterised Archaea (the halobac-

teria, methanogens and sulphur-reducing bac-

teria, formerly comprising the Archaebacteria),

the most basic photosynthetic organisms of the

phytoplankton belong to the Bacteria (formerly,

Eubacteria). The separation of the ancestral bac-

teria from the archaeans (distinguished by the

possession of membranes formed of branched

hydrocarbons and ether linkages, as opposed to

the straight-chain fatty acids and ester linkages

found in the membranes of all other organisms:

Atlas and Bartha, 1993) occurred early in micro-

bial evolution (Woese, 1987; Woese et al., 1990).

The appearance of phototrophic forms, dis-

tinguished by their crucial ability to use light

energy in order to synthesise adenosine triphos-

phate (ATP) (see Chapter 3), was also an ancient

event that took place some 3000 million years ago

(3 Ga BP (before present)). Some of these organ-

isms were photoheterotrophs, requiring organicprecursors for the synthesis of their own cells.

Modern forms include green flexibacteria (Chlo-

roflexaceae) and purple non-sulphur bacteria

(Rhodospirillaceae), which contain pigments sim-

ilar to chlorophyll (bacteriochlorophyll a, b or

c ). Others were true photoautotrophs, capable

of reducing carbon dioxide as a source of cell

carbon (photosynthesis). Light energy is used to

strip electrons from a donor substance. In most

modern plants, water is the source of reductant

electrons and oxygen is liberated as a by-product

(oxygenic photosynthesis). Despite their phyletic

proximity to the photoheterotrophs and shar-

ing a similar complement of bacteriochloro-

phylls (Béjà et al., 2002), the Anoxyphotobac-

teria use alternative sources of electrons and,

in consequence, generate oxidation products

other than oxygen (anoxygenic photosynthesis).

Their modern-day representatives are the purple

and green sulphur bacteria of anoxic sediments.

Some of these are planktic in the sense that

they inhabit anoxic, intensively stratified layers

deep in small and suitably stable lakes. The trait

might be seen as a legacy of having evolved in a

wholly anoxic world. However, aerobic, anoxy-

genic phototrophic bacteria, containing bac-

terichlorophyll a, have been isolated from oxic

marine environments (Shiba et al., 1979); it has

also become clear that their contribution to the

oceanic carbon cycle is not necessarily insignifi-

cant (Kolber et al., 2001; Goericke, 2002).

Nevertheless, the oxygenic photosynthesis pio-

neered by the Cyanobacteria from about 2.8 Ga before present has proved to be a crucial step in

the evolution of life in water and, subsequently,

on land. Moreover, the composition of the atmos-

phere was eventually changed through the biolo-

gical oxidation of water and the simultaneous

removal and burial of carbon in marine sedi-

ments (Falkowski, 2002). Cyanobacterial photo-

synthesis is mediated primarily by chlorophyll

a, borne on thylakoid membranes. Accessory


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6 PHYTOPLANKTON

Table 1.1 Survey of the organisms in the phytoplankton

Domain: BACTERIA

Division: Cyanobacteria (blue-green algae)

Unicellular and colonial bacteria, lacking membrane bound plastids. Primary

photosynthetic pigment is chlorophyll a, with accessory phycobilins (phycocyanin,

phycoerythrin). Assimilation products, glycogen, cyanophycin. Four main sub-groups,of which three have planktic representatives.

Order: CHROOCOCCALES

Unicellular or coenobial Cyanobacteria but never filamentous. Most planktic genera

form mucilaginous colonies, and these are mainly in fresh water. Picophytoplanktic

forms abundant in the oceans.

Includes: Aphanocapsa, Aphanothece, Chroococcus, Cyanodictyon,

Gomphosphaeria, Merismopedia, Microcystis, Snowella, Synechococcus,

Synechocystis, Woronichinia

Order: OSCILLATORIALES

Uniseriate–filamentous Cyanobacteria whose cells all undergo division in the same

plane. Marine and freshwater genera.Includes: Arthrospira, Limnothrix, Lyngbya, Planktothrix, Pseudanabaena, Spirulina,

Trichodesmium, Tychonema

Order: NOSTOCALES

Unbranched–filamentous Cyanobacteria whose cells all undergo division in the same

plane and certain of which may be facultatively differentiated into heterocysts. In the

plankton of fresh waters and dilute seas.

Includes: Anabaena, Anabaenopsis, Aphanizomenon, Cylindrospermopsis,

Gloeotrichia, Nodularia

Exempt Division: Prochlorobacteria

Order: PROCHLORALES

Unicellular and colonial bacteria, lacking membrane-bound plastids. Photosyntheticpigments are chlorophyll a and b, but lack phycobilins.

Includes: Prochloroccus, Prochloron, Prochlorothrix

Division: Anoxyphotobacteria

Mostly unicellular bacteria whose (anaerobic) photosynythesis depends upon an

electron donor other than water and so do not generate oxygen. Inhabit anaerobic

sediments and (where appropriate) water layers where light penetrates sufficiently.

Two main groups:

Family: Chromatiaceae (purple sulphur bacteria) Cells able to photosynthesise

with sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.

Includes: Chromatium, Thiocystis, Thiopedia.

Family: Chlorobiaceae (green sulphur bacteria) Cells able to photosynthesisewith sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.

Includes: Chlorobium, Clathrocystis, Pelodictyon.

Domain: EUCARYA

Phylum: Glaucophyta

Cyanelle-bearing organisms, with freshwater planktic representatives.

Includes: Cyanophora, Glaucocystis.

Phylum: Prasinophyta

Unicellular, mostly motile green algae with 1–16 laterally or apically placed flagella,

cell walls covered with fine scales and plastids containing chlorophyll a and b.

Assimilatory products mannitol, starch.

(cont.)


23/550


Table 1.1 (cont.)

CLASS: Pedinophyceae

Order: PEDINOMONADALES

Small cells, with single lateral flagellum.

Includes: Pedinomonas

CLASS: PrasinophyceaeOrder: CHLORODENDRALES

Flattened, 4-flagellated cells.

Includes: Nephroselmis, Scherffelia (freshwater); Mantoniella, Micromonas

(marine)

Order: PYRAMIMONADALES

Cells with 4 or 8 (rarely 16) flagella arising from an anterior depression. Marine

and freshwater.

Includes: Pyramimonas

Order: SCOURFIELDIALES

Cells with two, sometimes unequal, flagella. Known from freshwater ponds.

Includes: ScourfieldiaPhylum: Chlorophyta (green algae)

Green-pigmented, unicellular, colonial, filamentous, siphonaceous and thalloid

algae. One or more chloroplasts containing chlorophyll a and b. Assimilation

product, starch (rarely, lipid).

CLASS: Chlorophyceae

Several orders of which the following have planktic representatives:

Order: TETRASPORALES

Non-flagellate cells embedded in mucilaginous or palmelloid colonies, but with

motile propagules.

Includes: Paulschulzia, Pseudosphaerocystis

Order: VOLVOCALESUnicellular or colonial biflagellates, cells with cup-shaped chloroplasts.

Includes: Chlamydomonas, Eudorina, Pandorina, Phacotus, Volvox (in fresh

waters); Dunaliella, Nannochloris (marine)

Order: CHLOROCOCCALES

Non-flagellate, unicellular or coenobial (sometimes mucilaginous) algae, with

many planktic genera.

Includes: Ankistrodesmus, Ankyra, Botryococcus, Chlorella,

Coelastrum, Coenochloris, Crucigena, Choricystis, Dictyosphaerium,

Elakatothrix, Kirchneriella, Monorophidium, Oocystis, Pediastrum,

Scenedesmus, Tetrastrum

Order: ULOTRICHALESUnicellular or mostly unbranched filamentous with band-shaped chloroplasts.

Includes: Geminella, Koliella, Stichococcus

Order: ZYGNEMATALES

Unicellular or filamentous green algae, reproducing isogamously by conjugation.

Planktic genera are mostly members of the Desmidaceae, mostly unicellular or

(rarely) filmentous coenobia with cells more or less constricted into two

semi-cells linked by an interconnecting isthmus. Exclusively freshwater genera.

Includes: Arthrodesmus, Closterium, Cosmarium, Euastrum, Spondylosium,

Staurastrum, Staurodesmus, Xanthidium

(cont.)


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8 PHYTOPLANKTON

Table 1.1 (cont.)

Phylum: Euglenophyta

Green-pigmented unicellular biflagellates. Plastids numerous and irregular,

containing chlorophyll a and b. Reproduction by longitudinal fission. Assimilation

product, paramylon, oil. One Class, Euglenophyceae, with two orders.

Order: EUTREPTIALESCells having two emergent flagella, of approximately equal length. Marine and

freshwater species.

Includes: Eutreptia

Order: EUGLENALES

Cells having two flagella, one very short, one long and emergent.

Includes: Euglena, Lepocinclis, Phacus, Trachelmonas

Phylum: Cryptophyta

Order: CRYPTOMONADALES

Naked, unequally biflagellates with one or two large plastids, containing

chlorophyll a and c2 (but not chlorophyll b); accessory phycobiliproteins or other

pigments colour cells brown, blue, blue-green or red; assimilatory product,starch. Freshwater and marine species.

Includes: Chilomonas, Chroomonas, Cr yptomonas, Plagioselmis, Pyrenomonas,

Rhodomonas

Phylum: Raphidophyta

Order: RAPHIDOMONADALES (syn. CHLOROMONADALES)

Biflagellate, cellulose-walled cells; two or more plastids containing chlorophyll a;

cells yellow-green due to predominant accessory pigment, diatoxanthin;

assimilatory product, lipid. Freshwater.

Includes: Gonyostomum

Phylum: Xanthophyta (yellow-green algae)

Unicellular, colonial, filamentous and coenocytic algae. Motile species generally subapically and unequally biflagellated; two or many more discoid plastids per cell

containing chlorophyll a. Cells mostly yellow-green due to predominant

accessory pigment, diatoxanthin; assimilation product, lipid. Several orders, two

with freshwater planktic representatives.

Order: MISCHOCOCCALES

Rigid-walled, unicellular, sometimes colonial xanthophytes.

Includes: Goniochloris, Nephrodiella, Ophiocytium

Order: TRIBONEMATALES

Simple or branched uniseriate filamentous xanthophytes.

Includes: Tribonema

Phylum: EustigmatophytaCoccoid unicellular, flagellated or unequally biflagellated yellow-green algae with

masking of chlorophyll a by accessory pigment violaxanthin. Assimilation product,

probably lipid.

Includes: Chlorobotrys, Monodus

Phylum: Chrysophyta (golden algae)

Unicellular, colonial and filamentous. often uniflagellate, or unequally biflagellate

algae. Contain chlorophyll a, c1 and c2, generally masked by abundant accessory

pigment, fucoxanthin, imparting distinctive golden colour to cells. Cells

sometimes naked or or enclosed in an urn-shaped lorica, sometimes with

siliceous scales. Assimilation products, lipid, leucosin. Much reclassified group, has

several classes and orders in the plankton. (cont.)


25/550


Table 1.1 (cont.)

CLASS: Chrysophyceae

Order: CHROMULINALES

Mostly planktic, unicellular or colony-forming flagellates with one or two

unequal flagella, occasionally naked, often in a hyaline lorica or gelatinous

envelope.Includes: Chromulina, Chrysococcus, Chrysolykos, Chrysosphaerella, Dinobryon,

Kephyrion, Ochromonas, Uroglena

Order: HIBBERDIALES

Unicellular or colony-forming epiphytic gold algae but some planktic

representatives.

Includes: Bitrichia

CLASS: Dictyochophyceae

Order: PEDINELLALES

Radially symmetrical, very unequally biflagellate unicells or coenobia.

Includes: Pedinella (freshwater); Apedinella, Pelagococcus, Pelagomonas,

Pseudopedinella (marine)CLASS: Synurophyceae

Order: SYNURALES

Unicellular or colony-forming flagellates, bearing distinctive siliceous scales.

Includes: Mallomonas, Synura

Phylum: Bacillariophyta (diatoms)

Unicellular and coenobial yellow-brown, non-motile algae with numerous discoid

plastids, containing chlorophyll a, c1 and c2, masked by accessory pigment,

fucoxanthin. Cell walls pectinaceous, in two distinct and overlapping halves, and

impregnated with cryptocrystalline silica. Assimilatory products, chrysose, lipids.

Two large orders, both conspicuously represented in the marine and freshwater

phytoplankton.CLASS: Bacillariophyceae

Order: BIDDULPHIALES (centric diatoms)

Diatoms with cylindrical halves, sometimes well separated by girdle bands. Some

species form (pseudo-)filaments by adhesion of cells at their valve ends.

Includes: Aulacoseira, Cyclotella, Stephanodiscus, Urosolenia (freshwater);

Cerataulina, Chaetoceros, Detonula, Rhizosolenia, Skeletonema, Thalassiosira

(marine)

Order: BACILLARIALES (pennate diatoms)

Diatoms with boat-like halves, no girdle bands. Some species form coenobia by

adhesion of cells on their girdle edges.

Includes: Asterionella, Diatoma, Fragilaria, Synedra, Tabellaria (freshwater); Achnanthes, Fragilariopsis, Nitzschia (marine)

Phylum: Haptophyta

CLASS: Haptophyceae

Gold or yellow-brown algae, usually unicellular, with two subequal flagella and a

coiled haptonema, but with amoeboid, coccoid or palmelloid stages. Pigments,

chlorophyll a, c1 and c2, masked by accessory pigment (usually fucoxanthin).

Assimilatory product, chrysolaminarin. Cell walls with scales, sometimes more or

less calcified.

Order: PAVLOVALES

Cells with haired flagella and small haptonema. Marine and freshwater species.

Includes: Diacronema, Pavlova (cont.)


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10 PHYTOPLANKTON

Table 1.1 (cont.)

Order: PRYMNESIALES

Cells with smooth flagella, haptonema usually small. Mainly marine or brackish

but some common in freshwater plankton.

Includes: Chrysochromulina, Isochrysis, Phaeocystis, Prymnesium

Order: COCCOLITHOPHORIDALESCell suface covered by small, often complex, flat calcified scales (coccoliths).

Exclusively marine.

Include: Coccolithus, Emiliana, Florisphaera, Gephyrocapsa, Umbellosphaera

Phylum: Dinophyta

Mostly unicellular, sometimes colonial, algae with two flagella of unequal length

and orientation. Complex plastids containing chlorophyll a, c1 and c2, generally

masked by accessory pigments. Cell walls firm, or reinforced with polygonal

plates. Assimilation products: starch, oil. Conspicuously represented in marine

and freshwater plankton. Two classes and (according to some authorities) up to

11 orders.

CLASS: DinophyceaeBiflagellates, with one transverse flagellum encircling the cell, the other directed

posteriorly.

Order: GYMNODINIALES

Free-living, free-swimming with flagella located in well-developed transverse and

sulcal grooves, without thecal plates. Mostly marine.

Includes: Amphidinium, Gymnodinium, Woloszynskia

Order: GONYAULACALES

Armoured, plated, free-living unicells, the apical plates being asymmetrical.

Marine and freshwater.

Includes: Ceratium, Lingulodinium

Order: PERIDINIALESArmoured, plated, free-living unicells, with symmetrical apical plates. Marine and

freshwater.

Includes: Glenodinium, Gyrodinium, Peridinium

Order: PHYTODINIALES

Coccoid dinoflagellates with thick cell walls but lacking thecal plates. Many

epiphytic for part of life history. Some in plankton of humic fresh waters.

Includes: Hemidinium

CLASS: Adinophyceae

Order: PROROCENTRALES

Naked or cellulose-covered cells comprising two watchglass-shaped halves.

Marine and freshwater species.Includes: Exuviella, Prorocentrum

pigments, called phycobilins, are associated with

these membranes, where they are carried in

granular phycobilisomes. Life forms among the

Cyanobacteria have diversified from simple coc-

coids and rods into loose mucilaginous colonies,

called coenobia, into filamentous and to pseu-

dotissued forms. Four main evolutionary lines

are recognised, three of which (the chroococ-

calean, the oscillatorialean and the nostocalean;

the stigonematalean line is the exception) have

major planktic representatives that have diversi-

fied greatly among marine and freshwater sys-

tems. The most ancient group of the surviv-

ing groups of photosynthetic organisms is, in


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THE DIVERSIFICATION OF PHYTOPLANKTON 1

terms of individuals, the most abundant on the

planet.

Links to eukaryotic protists, plants and ani-

mals from the Cyanobacteria had been sup-

posed explicitly and sought implicitly. The dis-

covery of a prokaryote containing chlorophyll a

and b but lacking phycobilins, thus resemblingthe pigmentation of green plants, seemed to

fit the bill (Lewin, 1981). Prochloron, a symbiont

of salps, is not itself planktic but is recover-

able in collections of marine plankton. The first

description of Prochlorothrix from the freshwa-

ter phytoplankton in the Netherlands (Burger-

Wiersma et al., 1989) helped to consolidate the

impression of an evolutionary ‘missing link’ of

chlorophyll-a- a n d -b-containing bacteria. Then

came another remarkable finding: the most

abundant picoplankter in the low-latitude ocean

was not a Synechococcus, as had been thitherto sup-

posed, but another oxyphototrophic prokaryote

containing divinyl chlorophyll-a and -b pigments

but no bilins (Chisholm et al., 1988, 1992); it was

named Prochlorococcus. The elucidation of a bio-

spheric role of a previously unrecognised organ-

ism is achievement enough by itself (Pinevich

et al., 2000); for the organisms apparently to

occupy this transitional position in the evolu-

tion of plant life doubles the sense of scientific

satisfaction. Nevertheless, subsequent investiga-

tions of the phylogenetic relationships of the

newly defined Prochlorobacteria, using immuno-

logical and molecular techniques, failed to group

Prochlorococcus with the other Prochlorales or even

to separate it distinctly from Synechococcus (Moore

et al., 1998; Urbach et al., 1998). The present view

is that it is expedient to regard the Prochlorales

as aberrent Cyanobacteria (Lewin, 2002).

The common root of all eukaryotic algae and

higher plants is now understood to be basedupon original primary endosymbioses involv-

ing early eukaryote protistans and Cyanobacteria

(Margulis, 1970, 1981). As more is learned about

the genomes and gene sequences of microorgan-

isms, so the role of ‘lateral’ gene transfers in

shaping them is increasingly appreciated (Doolit-

tle et al., 2003). For instance, in terms of ultra-

structure, the similarity of 16S rRNA sequences,

several common genes and the identical pho-

tosynthetic proteins, all point to cyanobacterial

origin of eukaruote plastids (Bhattacharya and

Medlin, 1998; Douglas and Raven, 2003). Prag-

matically, we may judge this to have been a

highly successful combination. There may well

have been others of which nothing is known,

apart from the small group of glaucophytes that

carry cyanelles rather than plastids. The cyanellesare supposed to be an evolutionary interme-

diate between cyanobacterial cells and chloro-

plasts (admittedly, much closer to the latter).

Neither cyanelles nor plastids can grow inde-

pendently of the eukaryote host and they are

apportioned among daughters when the host cell

divides. There is no evidence that the handful

of genera ascribed to this phylum are closely

related to each other, so it may well be an arti-

ficial grouping. Cyanophora is known from the

plankton of shallow, productive calcareous lakes

(Whitton in John et al., 2002).

Molecular investigation has revealed that the

seemingly disparate algal phyla conform to one

or other of two main lineages. The ‘green line’

of eukaryotes with endosymbiotic Cyanobacteria

reflects the development of the chlorophyte and

euglenophyte phyla and to the important off-

shoots to the bryophytes and the vascular plant

phyla. The ‘red line’, with its secondary and even

tertiary endosymbioses, embraces the evolution

of the rhodophytes, the chrysophytes and the

haptophytes, is of equal or perhaps greater fas-

cination to the plankton ecologist interested in

diversity.

A key distinguishing feature of the algae of

the green line is the inclusion of chlorophyll

b among the photosynthetic pigments and, typ-

ically, the accumulation of glucose polymers

(such as starch, paramylon) as the main prod-

uct of carbon assimilation. The subdivision of

the green algae between the prasinophyte andthe chlorophyte phyla reflects the evolutionary

development and anatomic diversification within

the line, although both are believed to have

a long history on the planet (∼1.5 Ga). Bothare also well represented by modern genera, in

water generally and in the freshwater phyto-

plankton in particular. Of the modern prasino-

phyte orders, the Pedinomonadales, the Chloro-

dendrales and the Pyramimonadales each have

significant planktic representation, in the sense


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12 PHYTOPLANKTON

of producing populations of common occurrence

and forming ‘blooms’ on occasions. Several mod-

ern chlorophyte orders (including Oedogoniales,

Chaetophorales, Cladophorales, Coleochaetales,

Prasiolales, Charales, Ulvales a.o.) are without

modern planktic representation. In contrast,

there are large numbers of volvocalean, chloro-coccalean and zygnematalean species in lakes

and ponds and the Tetrasporales and Ulotrichales

are also well represented. These show a very wide

span of cell size and organisation, with flagel-

lated and non-motile cells, unicells and filamen-

tous or ball-like coenobia, with varying degrees of

mucilaginous investment and of varying consis-

tency. The highest level of colonial development

is arguably in Volvox, in which hundreds of net-

worked biflagellate cells are coordinated to bring

about the controlled movement of the whole.

Colonies also reproduce by the budding off and

release of near-fully formed daughter colonies.

The desmid members of the Zygnematales are

amongst the best-studied green plankters. Mostly

unicellular, the often elaborate and beautiful

architecture of the semi-cells invite the gaze and

curiosity of the microscopist.

The euglenoids are unicellular flagellates.

A majority of the 800 or so known species

are colourless heterotrophs or phagotrophs and

are placed by zoologists in the protist order

Euglenida. Molecular investigations reveal them

to be a single, if disparate group, some of which

acquired the phototrophic capability through

secondary symbioses. It appears that even the

phototrophic euglenoids are capable of absorb-

ing and assimilating particular simple organic

solutes. Many of the extant species are associ-

ated with organically rich habitats (ponds and

lagoons, lake margins, sediments).

The ‘red line’ of eukaryotic evolution is basedon rhodophyte plastids that contain phycobilins

and chlorophyll a, and whose single thylakoids

lie separately and regularly spaced in the plastid

stroma (see, e.g., Kirk, 1994). The modern phy-

lum Rhodophyta is well represented in marine

(especially; mainly as red seaweeds) and fresh-

water habitats but no modern or extinct plank-

tic forms are known. However, among the inter-

esting derivative groups that are believed to

owe to secondary endosymbioses of rhodophyte

cells, there is a striking variety of planktic

forms.

Closest to the ancestral root are the cryp-

tophytes. These contain chlorophyll c 2, as well

as chlorophyll a and phycobilins, in plastid thy-

lakoids that are usually paired. Living cells are

generally green but with characteristic, species-specific tendencies to be bluish, reddish or

olive-tinged. The modern planktic representatives

are exclusively unicellular; they remain poorly

known, partly because thay are not easy to

identify by conventional means. However, about

100 species each have been named for marine

and fresh waters, where, collectively, they occur

widely in terms of latitude, trophic state and

season.

Next comes the small group of single-

celled flagellates which, despite showing similar-

ities with the cryptophytes, dinoflagellates and

euglenophytes, are presently distinguished in the

phylum Raphidophyta. One genus, Gonyostomum,

is cosmopolitan and is found, sometimes in abun-

dance, in acidic, humic lakes. The green colour

imparted to these algae by chlorophyll a is, to

some extent, masked by a xanthophyll (in this

case, diatoxanthin) to yield the rather yellowish

pigmentation. This statement applies even more

to the yellow-green algae making up the phyla

Xanthophyta and Eustigmatophyta. The xantho-

phytes are varied in form and habit with a

number of familiar unicellular non-flagellate or

biflagellate genera in the freshwater plankton, as

well as the filamentous Tribonema of hard-water

lakes. The eustigmatophytes are unicellular coc-

coid flagellates of uncertain affinities that take

their name from the prominent orange eye-spots.

The golden algae (Chrysophyta) represent a

further recombination along the red line, giv-

ing rise to a diverse selection of modern unicel-lular, colonial or filamentous algae. With a dis-

tinctive blend of chlorophyll a, c 1 and c 2, and the

major presence of the xanthophyll fucoxanthin,

the chrysophytes are presumed to be close to

the Phaeophyta, which includes all the macro-

phytic brown seaweeds but no planktic vege-

tative forms. Most of the chrysophytes have,

in contrast, remained microphytic, with numer-

ous planktic genera. A majority of these come

from fresh water, where they are traditionally


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THE DIVERSIFICATION OF PHYTOPLANKTON 1

supposed to indicate low nutrient status and pro-

ductivity (but see Section 3.4.3: they may simply

be unable to use carbon sources other than car-

bon dioxide). Mostly unicellular or coenobial flag-

ellates, many species are enclosed in smooth

protective loricae, or they may be beset with

numerous delicate siliceous scales. The group has been subject to considerable taxonomic revision

and reinterpretation of its phylogenies in recent

years. The choanoflagellates (formerly Craspedo-

phyceae, Order Monosigales) are no longer con-

sidered to be allied to the Chrysophytes.

The last three phyla named in Table 1.1,

each conspicuously represented in both limnetic

and marine plankton – indeed, they are the

main pelagic eukaryotes in the oceans – are

also remarkable in having relatively recent ori-

gins, in the mesozoic period. The Bacillariophyta

(the diatoms) is a highly distinctive phylum of

single cells, filaments and coenobia. The char-

acteristics are the possession of golden-brown

plastids containing the chlorophylls a, c 1 and

c 2 and the accessory pigment fucoxanthin, and

the well-known presence of a siliceous frustule

or exoskeleton. Generally, the latter takes the

form of a sort of lidded glass box, with one of

two valves fitting in to the other, and bound by

one or more girdle bands. The valves are often

patterned with grooves, perforations and callosi-

ties in ways that greatly facilitate identification.

Species are ascribed to one or other of the two

main diatom classes. In the Biddulphiales, or

centric diatoms, the valves are usually cylindri-

cal, making a frustule resembling a traditional

pill box; in the Bacillariales, or pennate diatoms,

the valves are elongate but the girdles are short,

having the appearance of the halves of a date

box. While much is known and has been writ-

ten on their morphology and evolution (see, forinstance, Round et al., 1990), the origin of the

siliceous frustule remains obscure.

The Haptophyta are typically unicellular gold

or yellow-brown algae, though having amoeboid,

coccoid or palmelloid stages in some cases. The

pigment blend of chlorophylls a, c 1 and c 2,

with accessory fucoxanthin, resembles that of

other gold-brown phyla. The haptophytes are dis-

tinguished by the possession of a haptonema,

located between the flagella. In some species it

is a prominent thread, as long as the cell; in oth-

ers it is smaller or even vestigial but, in most

instances, can be bent or coiled. Most of the

known extant haptophyte species are marine;

some genera, such as Chrysochromulina, are rep-

resented by species that are relatively frequent

members of the plankton of continental shelvesand of mesotrophic lakes. Phaeocystis is another

haptophyte common in enriched coastal waters,

where it may impart a visible yellow-green colour

to the water at times, and give a notoriously slimy

texture to the water (Hardy, 1964).

The coccolithophorids are exclusively marine

haptophytes and among the most distinctive

microorganisms of the sea. They have a charac-

teristic surface covering of coccoliths – flattened,

often delicately fenestrated, scales impregnated

with calcium carbonate. They fossilise particu-

larly well and it is their accumulation which

mainly gave rise to the massive deposits of chalk

that gave its name to the Cretaceous (from Greek

kreta, chalk) period, 120–65 Ma BP. Modern coc-

colithophorids still occur locally in sufficient pro-

fusion to generate ‘white water’ events. One of

the best-studied of the modern coccolithophorids

is Emiliana.

The final group in this brief survey is the

dinoflagellates. These are mostly unicellular,

rarely colonial biflagellated cells; some are rel-

atively large (up to 200 to 300 µ m across) and

have complex morphology. Pigmentation gener-

ally, but not wholly, reflects a red-line ancestry,

the complex plastids containing chlorophyll a,

c 1 and c 2 and either fucoxanthin or peridinin

as accessory pigments, possibly testifying to ter-

tiary endosymbioses (Delwiche, 2000). The group

shows an impressive degree of adaptive radia-

tion, with naked gymnodinioid nanoplankters

through to large, migratory gonyaulacoid swim-mers armoured with sculpted plates and to deep-

water shade forms with smooth cellulose walls

such as Pyrocystis. Some genera are non-planktic

and even pass part of the life cycle as epiphytes.

Freshwater species of Ceratium and larger species

of Peridinium are conspicuous in the plankton

of certain types of lakes during summer strati-

fication, while smaller species of Peridinium and

other genera (e.g. Glenodinium) are associated with

mixed water columns of shallow ponds.


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14 PHYTOPLANKTON

Figure 1.1 Non-motile

unicellular phytoplankters.

(a) Synechococcus sp.; (b ) Ankyra

judayi ; (c) Stephanodiscus rotula;

(d) Closterium cf. acutum. Scale bar,

10 µ m. Original photomicrographs

by Dr H. M. Canter-Lund,reproduced from Reynolds (1984a).

The relatively recent appearance of diatoms,

coccolithophorids and dinoflagellates in the

fossil record provides a clear illustration of

how evolutionary diversification comes about.

Although it cannot be certain that any of these

three groups did not exist beforehand, there

is no doubt about their extraordinary rise dur-ing the Mesozoic. The trigger may well have

been the massive extinctions towards the end of

the Permian period about 250 Ma BP, when a

huge release of volcanic lava, ash and shroud-

ing dust from what is now northern Siberia

brought about a world-wide cooling. The trend

was quickly reversed by accumulating atmo-

spheric carbon dioxide and a period of severe

global warming (which, with positive feedback

of methane mobilisation from marine sediments,

raised ambient temperatures by as much as

10–11 ◦C). Life on Earth suffered a severe set- back, perhaps as close as it has ever come

to total eradication. In a period of less than

0.1 Ma, many species fell extinct and the sur-

vivors were severely curtailed. As the planet

cooled over the next 20 or so million years,

the rump biota, on land as in water, were ableto expand and radiate into habitats and niches

that were otherwise unoccupied (Falkowski,

2002).

Dinoflagellate fossils are found in the early

Triassic, the coccolithophorids from the late Tri-

assic (around 180 Ma BP). Together with the

diatoms, many new species appeared in the Juras-

sic and Cretaceous periods. In the sea, these three

groups assumed a dominance over most other

forms, the picocyanobacteria excluded, which

persists to the present day.


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GENERAL FEATURES OF PHYTOPLANKTON 1

Figure 1.2 Planktic unicellular

flagellates. (a) Two variants of

Ceratium hirundinella; (b)

overwintering cyst of Ceratium

hirundinella, with vegetative cell for

comparison; (c) empty case of

Peridinium willei to show exoskeletalplates and flagellar grooves; (d)

Mallomonas caudata; (e) Plagioselmis

nannoplanctica; (f) two cells of

Cryptomonas ovata; (g) Phacus

longicauda; (h) Euglena sp.; (j)

Trachelomonas hispida. Scale bar, 10

µ m. Original photomicrographs by

Dr H. M. Canter-Lund, reproduced

from Reynolds (1984a).

1.4 General features of phytoplankton

Despite being drawn from a diverse range of

what appear to be distantly related phyloge-

netic groups (Table 1.1), there are features that

phytoplankton share in common. In an earlier

book (Reynolds, 1984a), I suggested that these

features reflected powerful convergent forces in

evolution, implying that the adaptive require-

ments for a planktic existence had risen inde-

pendently within each of the major phyla repre-

sented. This may have been a correct deduction,

although there is no compelling evidence that

it is so. On the other hand, for small, unicellu-

lar microorganisms to live freely in suspension

in water is an ancient trait, while the transition

to a full planktic existence is seen to be a rel-

atively short step. It remains an open question

whether the supposed endosymbiotic recombina-

tions could have occurred in the plankton, or

whether they occurred among other precursors

that subsequently established new lines of plank-

tic invaders.

It is not a problem that can yet be answered

satisfactorily. However, it does not detract from

the fact that to function and survive in the

plankton does require some specialised adapta-

tions. It is worth emphasising again that just as

phytoplankton comprises organisms other than

algae, so not all algae (or even very many of

them) are necessarily planktic. Moreover, neither

the shortness of the supposed step to a plank-tic existence nor the generally low level of struc-

tural complexity of planktic unicells and coeno-

bia should deceive us that they are necessarily

simple organisms. Indeed, much of this book

deals with the problems of life conducted in a

fluid environment, often in complete isolation

from solid boundaries, and the often sophisti-

cated means by which planktic organisms over-

come them. Thus, in spite of the diversity of phy-

logeny (Table 1.1), even a cursory consideration

of the range of planktic algae (see Figs. 1.1–1.5)


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16 PHYTOPLANKTON

Figure 1.3 Coenobial

phytoplankters. Colonies of the

diatoms (a) Asterionella formosa, (b)

Fragilaria crotonensis and (d) Tabellaria

flocculosa var. asterionelloides. The

fenestrated colony of the

chlorophyte Pediastrum duplex isshown in (c). Scale bar, 10 µ m.

Original photomicrographs by Dr

H. M. Canter-Lund, reproduced

from Reynolds (1984a).

reveals a commensurate diversity of form, func-

tion and adaptive strategies.

What features, then, are characteristic and

common to phytoplankton, and how have they

been selected? The overriding requirements of

any organism are to increase and multiply its

kind and for a sufficient number of the progeny

to survive for long enough to be able to invest

in the next generation. For the photoautotroph,

this translates to being able to fix sufficient car-

bon and build sufficient biomass to form the

next generation, before it is lost to consumersor to any of the several other potential fates that

await it. For the photoautotroph living in water,

the important advantages of archimedean sup-

port and the temperature buffering afforded by

the high specific heat of water (for more, see

Chapter 2) must be balanced against the diffi-

cuties of absorbing sufficient nutriment from

often very dilute solution (the subject of Chapter

4) and of intercepting sufficient light energy to

sustain photosynthetic carbon fixation in excess

of immediate respiratory needs (Chapter 3). How-

ever, radiant energy of suitable wavelengths

( photosynthetically active radiation, or PAR) is nei-

ther universally or uniformly available in water

but is sharply and hyperbolically attenuated with

depth, through its absorption by the water and

scattering by particulate matter (to be discussed

in Chapter 3). The consequence is that for a

given phytoplankter at anything more than a

few meters in depth, there is likely to be a crit-

ical depth (the compensation point ) below which

net photosynthetic accumulation is impossible.It follows that the survival of the phytoplankter

depends upon its ability to enter or remain in

the upper, insolated part of the water mass for

at least part of its life.

This much is well understood and the point

has been emphasised in many other texts. These

have also proffered the view that the essential

characteristic of a planktic photoautotroph is to

minimise its rate of sinking. This might be liter-

ally true if the water was static (in which case,


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GENERAL FEATURES OF PHYTOPLANKTON 1

Figure 1.4 Filamentous

phytoplankters. Filamentous

coenobia of the diatom Aulacoseira

subarctica (a,

ecology of phytoplankton 2006

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