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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 the
main 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.
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 va t i o n
Series editors
Michael Usher University of Stirling, and formerly Scottish Natural Heritage
Denis Saunders Formerly CSIRO Division of Sustainable Ecosystems, Canberra
Robert Peet University of North Carolina, Chapel Hill
Andrew Dobson Princeton University
Editorial Board
Paul Adam University of New South Wales, Australia
H. J. B. Birks University of Bergen, Norway
Lena Gustafsson Swedish University of Agricultural Science
Jeff McNeely International Union for the Conservation of Nature
R. T. Paine University of Washington
David Richardson University of Cape Town
Jeremy Wilson Royal Society for the Protection of Birds
The world’s biological diversity faces unprecedented threats. The urgent challenge facing the 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
The Ecology of Phytoplankton
C. S. Reynolds
cambridge university press
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo
Cambridge University Press
The Edinburgh Building, Cambridge cb2 2ru, UK
First published in print format
isbn-13 978-0-521-84413-0
isbn-13 978-0-521-60519-9
isbn-13 978-0-511-19094-0
© 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.
isbn-10 0-511-19094-8
isbn-10 0-521-84413-4
isbn-10 0-521-60519-9
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guarantee 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
hardback
paperback
paperback
eBook (EBL)
eBook (EBL)
hardback
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 Ramo´n Margalef. Each is
a constant source of inspiration to me.
Contents
Preface page ix
Acknowledgements xii
Chapter 1. Phytoplankton 1
1.1 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 38
2.1 Introduction 38
2.2 Motion in aquatic environments 39
2.3 Turbulence 42
2.4 Phytoplankton sinking and floating 49
2.5 Adaptive and evolutionary mechanisms for
regulating ws 53
2.6 Sinking and entrainment in natural turbulence 67
2.7 The spatial distribution of phytoplankton 77
2.8 Summary 90
Chapter 3. Photosynthesis and carbon acquisition in
phytoplankton 93
3.1 Introduction 93
3.2 Essential biochemistry of photosynthesis 94
3.3 Light-dependent environmental sensitivity of
photosynthesis 101
3.4 Sensitivity of aquatic photosynthesis to carbon
sources 124
3.5 Capacity, achievement and fate of primary
production at the ecosystem scale 131
3.6 Summary 143
Chapter 4. Nutrient uptake and assimilation in
phytoplankton 145
4.1 Introduction 145
4.2 Cell uptake and intracellular transport of
nutrients 146
4.3 Phosphorus: requirements, uptake, deployment in
phytoplankton 151
viii CONTENTS
4.4 Nitrogen: requirements, sources, uptake and
metabolism in phytoplankton 161
4.5 The role of micronutrients 166
4.6 Major ions 171
4.7 Silicon: requirements, uptake, deployment in
phytoplankton173
4.8 Summary 175
Chapter 5. Growth and replication of phytoplankton 178
5.1 Introduction: characterising growth 178
5.2 The mechanics and control of growth 179
5.3 The dynamics of phytoplankton growth and
replication in controlled conditions 183
5.4 Replication rates under sub-ideal conditions 189
5.5 Growth of phytoplankton in natural
environments 217
5.6 Summary 236
Chapter 6. Mortality and loss processes in phytoplankton 239
6.1 Introduction 239
6.2 Wash-out and dilution 240
6.3 Sedimentation 243
6.4 Consumption by herbivores 250
6.5 Susceptibility to pathogens and parasites 292
6.6 Death and decomposition 296
6.7 Aggregated impacts of loss processes on
phytoplankton composition 297
6.8 Summary 300
Chapter 7. Community assembly in the plankton: pattern,
process and dynamics 302
7.1 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 387
8.1 Introduction 387
8.2 Material transfers and energy flow in pelagic
systems 387
8.3 Anthropogenic change in pelagic environments 395
8.4 Summary 432
8.5 A last word 435
Glossary 437
Units, symbols and abbreviations 440
CONTENTS ix
References 447
Index to lakes, rivers and seas 508
Index to genera and species of
phytoplankton 511
Index to genera and species of other
organisms 520
General index 524
Preface
This is the third book I have written on the sub-
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. There
is 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
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 and
small-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 been
recognised, 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 appliesto 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 microbial
systems 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,
PREFACE xiii
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 Ramo´n
Margalef; I greatly enjoyed the opportunities to
discuss 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, Jo¨rg
Imberger, Petur Jo´nasson, Sven-Erik Jørgensen,
Dave Karl, Winfried Lampert, John Lawton, John
Raven, Marten Scheffer, Ted Smayda, Milan
Strasˇkraba, Reinhold Tu¨xen, 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 Ca´ceres, Paul Carling, Jean-Pierre Descy,
Mo´nica 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 Padisa´k, Fernando Pedrozo, Victor
Smetacˇek, 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 particular
times. 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), Siaˆn 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.
Acknowledgements
Except where stated, the illustrations in this book
are reproduced, redrawn or otherwise slightly
modified from sources noted in the individual
captions. 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 Cambridge
University 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 fu¨r theoretische und angewandte Limnolo-
gie by permission of Dr E. Na¨gele (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.
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 reveal
something 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 f loat
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 (<1 mm) size.
Crucially, this feature is mirrored in the fact
that the intrinsic movements of small organisms
are frequently too feeble to overcome the veloc-
ity and direction of much of the spectrum of
water movements. The inability to control hori-
zontal position or to swim against significant cur-
rents in open waters separates ‘plankton’ from
the ‘nekton’ of active swimmers, which include
adult fish, large cephalopods, aquatic reptiles,
birds and mammals.
2 PHYTOPLANKTON
Box 1.1 Some definitions used in the literaure
on plankton
seston the totality of particulate matter in water; all material not
in solution
tripton non-living seston
plankton living seston, adapted for a life spent wholly or partly in
quasi-suspension in open water, and whose powers of
motility do not exceed turbulent entrainment (see
Chapter 2)
nekton animals adapted to living all or part of their lives in open
water but whose intrinsic movements are almost
independent of turbulence
euplankton redundant term to distinguish fully adapted, truly planktic
organisms from other living organisms fortuitously
present in the water
tychoplankton non-adapted organisms from adjacent habitats and
present in the water mainly by chance
meroplankton planktic organisms passing a major part of the life history
out of the plankton (e.g. on the bottom sediments)
limnoplankton plankton of lakes
heleoplankton plankton of ponds
potamoplankton plankton of rivers
phytoplankton planktic photoautotrophs and major producer of the
pelagic
bacterioplankton planktic prokaryotes
mycoplankton planktic fungi
zooplankton planktic metazoa and heterotrophic protistans
Some more, now redundant, terms
The terms nannoplankton, ultraplankton, µ-algae are older names for various smaller
size categories of phytoplankton, eclipsed by the classification of Sieburth et al.
(1978) (see Box 1.2).
In this way, plankton comprises organisms
that range in size from that of viruses (a few tens
of 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 clear
that 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
HISTORICAL CONTEXT OF PHYTOPLANKTON STUDIES 3
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, adaptedto 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 their
article.
The existence of a planktic community of
organisms in open water had been demonstrated
many years previously by Johannes Mu¨ller. Knowl-
edge of some of the organisms themselves
stretches further back, to the earliest days
of microscopy. From the 1840s, Mu¨ller 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 Mu¨ller’s
assumption that the material floated up to the
surface waters – like so much oceanic dirt! It
took one of Mu¨ller’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
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
THE DIVERSIFICATION OF PHYTOPLANKTON 5
Box 1.2 The classification of phytoplankton according to
the scaling nomenclature of Sieburth et al. (1978)
Maximum linear dimension Namea
0.2–2 µm picophytoplankton
2–20 µm nanophytoplankton
20–200 µm microphytoplankton
200 µm–2 mm mesophytoplankton
>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 organic
precursors 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
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. Photosynthetic
pigments are chlorophyll a and b, but lack phycobilins.
Includes: Prochloroccus, Prochloron, Prochlorothrix
Division: Anoxyphotobacteria
Mostly unicellular bacteria whose (anaerobic) photosynythesis depends upon an
electron donor other than water and so do not generate oxygen. Inhabit anaerobic
sediments and (where appropriate) water layers where light penetrates sufficiently.
Two main groups:
Family: Chromatiaceae (purple sulphur bacteria) Cells able to photosynthesise
with sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.
Includes: Chromatium, Thiocystis, Thiopedia.
Family: Chlorobiaceae (green sulphur bacteria) Cells able to photosynthesise
with sulphide as sole electron donor. Cells contain bacteriochlorophyll a, b or c.
Includes: Chlorobium, Clathrocystis, Pelodictyon.
Domain: EUCARYA
Phylum: Glaucophyta
Cyanelle-bearing organisms, with freshwater planktic representatives.
Includes: Cyanophora, Glaucocystis.
Phylum: Prasinophyta
Unicellular, mostly motile green algae with 1–16 laterally or apically placed flagella,
cell walls covered with fine scales and plastids containing chlorophyll a and b.
Assimilatory products mannitol, starch.
(cont.)
THE DIVERSIFICATION OF PHYTOPLANKTON 7
Table 1.1 (cont.)
CLASS: Pedinophyceae
Order: PEDINOMONADALES
Small cells, with single lateral flagellum.
Includes: Pedinomonas
CLASS: Prasinophyceae
Order: CHLORODENDRALES
Flattened, 4-flagellated cells.
Includes: Nephroselmis, Scherffelia (freshwater); Mantoniella, Micromonas
(marine)
Order: PYRAMIMONADALES
Cells with 4 or 8 (rarely 16) flagella arising from an anterior depression. Marine
and freshwater.
Includes: Pyramimonas
Order: SCOURFIELDIALES
Cells with two, sometimes unequal, flagella. Known from freshwater ponds.
Includes: Scourfieldia
Phylum: Chlorophyta (green algae)
Green-pigmented, unicellular, colonial, filamentous, siphonaceous and thalloid
algae. One or more chloroplasts containing chlorophyll a and b. Assimilation
product, starch (rarely, lipid).
CLASS: Chlorophyceae
Several orders of which the following have planktic representatives:
Order: TETRASPORALES
Non-flagellate cells embedded in mucilaginous or palmelloid colonies, but with
motile propagules.Includes: Paulschulzia, Pseudosphaerocystis
Order: VOLVOCALES
Unicellular or colonial biflagellates, cells with cup-shaped chloroplasts.
Includes: Chlamydomonas, Eudorina, Pandorina, Phacotus, Volvox (in fresh
waters); Dunaliella, Nannochloris (marine)
Order: CHLOROCOCCALES
Non-flagellate, unicellular or coenobial (sometimes mucilaginous) algae, with
many planktic genera.
Includes: Ankistrodesmus, Ankyra, Botryococcus, Chlorella,
Coelastrum, Coenochloris, Crucigena, Choricystis, Dictyosphaerium,
Elakatothrix, Kirchneriella, Monorophidium, Oocystis, Pediastrum,
Scenedesmus, Tetrastrum
Order: ULOTRICHALES
Unicellular or mostly unbranched filamentous with band-shaped chloroplasts.
Includes: Geminella, Koliella, Stichococcus
Order: ZYGNEMATALES
Unicellular or filamentous green algae, reproducing isogamously by conjugation.
Planktic genera are mostly members of the Desmidaceae, mostly unicellular or
(rarely) filmentous coenobia with cells more or less constricted into two
semi-cells linked by an interconnecting isthmus. Exclusively freshwater genera.
Includes: Arthrodesmus, Closterium, Cosmarium, Euastrum, Spondylosium,
Staurastrum, Staurodesmus, Xanthidium
(cont.)
8 PHYTOPLANKTON
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: EUTREPTIALES
Cells having two emergent flagella, of approximately equal length. Marine and
freshwater species.
Includes: Eutreptia
Order: EUGLENALES
Cells having two flagella, one very short, one long and emergent.
Includes: Euglena, Lepocinclis, Phacus, Trachelmonas
Phylum: Cryptophyta
Order: CRYPTOMONADALES
Naked, unequally biflagellates with one or two large plastids, containing
chlorophyll a and c2 (but not chlorophyll b); accessory phycobiliproteins or other
pigments colour cells brown, blue, blue-green or red; assimilatory product,
starch. Freshwater and marine species.
Includes: Chilomonas, Chroomonas, Cryptomonas, Plagioselmis, Pyrenomonas,
Rhodomonas
Phylum: Raphidophyta
Order: RAPHIDOMONADALES (syn. CHLOROMONADALES)
Biflagellate, cellulose-walled cells; two or more plastids containing chlorophyll a;
cells yellow-green due to predominant accessory pigment, diatoxanthin;
assimilatory product, lipid. Freshwater.
Includes: Gonyostomum
Phylum: Xanthophyta (yellow-green algae)
Unicellular, colonial, filamentous and coenocytic algae. Motile species generally
subapically and unequally biflagellated; two or many more discoid plastids per cell
containing chlorophyll a. Cells mostly yellow-green due to predominant
accessory pigment, diatoxanthin; assimilation product, lipid. Several orders, two
with freshwater planktic representatives.
Order: MISCHOCOCCALES
Rigid-walled, unicellular, sometimes colonial xanthophytes.
Includes: Goniochloris, Nephrodiella, Ophiocytium
Order: TRIBONEMATALES
Simple or branched uniseriate filamentous xanthophytes.
Includes: Tribonema
Phylum: Eustigmatophyta
Coccoid unicellular, flagellated or unequally biflagellated yellow-green algae with
masking of chlorophyll a by accessory pigment violaxanthin. Assimilation product,
probably lipid.
Includes: Chlorobotrys, Monodus
Phylum: Chrysophyta (golden algae)
Unicellular, colonial and filamentous. often uniflagellate, or unequally biflagellate
algae. Contain chlorophyll a, c1 and c2, generally masked by abundant accessory
pigment, fucoxanthin, imparting distinctive golden colour to cells. Cells
sometimes naked or or enclosed in an urn-shaped lorica, sometimes with
siliceous scales. Assimilation products, lipid, leucosin. Much reclassified group, has
several classes and orders in the plankton.
(cont.)
THE DIVERSIFICATION OF PHYTOPLANKTON 9
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.)
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: COCCOLITHOPHORIDALES
Cell suface covered by small, often complex, flat calcified scales (coccoliths).
Exclusively marine.
Include: Coccolithus, Emiliana, Florisphaera, Gephyrocapsa, Umbellosphaera
Phylum: Dinophyta
Mostly unicellular, sometimes colonial, algae with two flagella of unequal length
and orientation. Complex plastids containing chlorophyll a, c1 and c2, generally
masked by accessory pigments. Cell walls firm, or reinforced with polygonal
plates. Assimilation products: starch, oil. Conspicuously represented in marine
and freshwater plankton. Two classes and (according to some authorities) up to
11 orders.
CLASS: Dinophyceae
Biflagellates, with one transverse flagellum encircling the cell, the other directed
posteriorly.
Order: GYMNODINIALES
Free-living, free-swimming with flagella located in well-developed transverse and
sulcal grooves, without thecal plates. Mostly marine.
Includes: Amphidinium, Gymnodinium, Woloszynskia
Order: GONYAULACALES
Armoured, plated, free-living unicells, the apical plates being asymmetrical.
Marine and freshwater.
Includes: Ceratium, Lingulodinium
Order: PERIDINIALES
Armoured, plated, free-living unicells, with symmetrical apical plates. Marine and
freshwater.
Includes: Glenodinium, Gyrodinium,Peridinium
Order: PHYTODINIALES
Coccoid dinoflagellates with thick cell walls but lacking thecal plates. Many
epiphytic for part of life history. Some in plankton of humic fresh waters.
Includes: Hemidinium
CLASS: Adinophyceae
Order: PROROCENTRALES
Naked or cellulose-covered cells comprising two watchglass-shaped halves.
Marine and freshwater species.
Includes: Exuviella, Prorocentrum
pigments, called phycobilins, are associated with
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
THE DIVERSIFICATION OF PHYTOPLANKTON 11
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 resembling
the 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- and -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 based
upon 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 cyanelles
are 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 and
the 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). Both
are 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
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 based
on 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 theinter-
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 c2, 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, c1 and c2, 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
THE DIVERSIFICATION OF PHYTOPLANKTON 13
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, c1 and
c2 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, for
instance, 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, c1 and c2,
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 shelves
and 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 µm across) and
have complex morphology. Pigmentation gener-
ally, but not wholly, reflects a red-line ancestry,
the complex plastids containing chlorophyll a,
c1 and c2 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.
14 PHYTOPLANKTON
Figure 1.1 Non-motile
unicellular phytoplankters.
(a) Synechococcus sp.; (b) Ankyra
judayi; (c) Stephanodiscus rotula;
(d) Closterium cf. acutum. Scale bar,
10 µm. Original photomicrographs
by Dr H. M. Canter-Lund,
reproduced from Reynolds (1984a).
The relatively recent appearance of diatoms,
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 trendwas 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 able
to 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.
GENERAL FEATURES OF PHYTOPLANKTON 15
Figure 1.2 Planktic unicellular
flagellates. (a) Two variants of
Ceratium hirundinella; (b)
overwintering cyst of Ceratium
hirundinella, with vegetative cell for
comparison; (c) empty case of
Peridinium willei to show exoskeletal
plates and flagellar grooves; (d)
Mallomonas caudata; (e) Plagioselmis
nannoplanctica; (f) two cells of
Cryptomonas ovata; (g) Phacus
longicauda; (h) Euglena sp.; (j)
Trachelomonas hispida. Scale bar, 10
µm. Original photomicrographs by
Dr H. M. Canter-Lund, reproduced
from Reynolds (1984a).
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)
16 PHYTOPLANKTON
Figure 1.3 Coenobial
phytoplankters. Colonies of the
diatoms (a) Asterionella formosa, (b)
Fragilaria crotonensis and (d) Tabellaria
flocculosa var. asterionelloides. The
fenestrated colony of the
chlorophyte Pediastrum duplex is
shown in (c). Scale bar, 10 µm.
Original photomicrographs by Dr
H. M. Canter-Lund, reproduced
from Reynolds (1984a).
reveals a commensurate diversity of form, func-
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 consumers
or 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,
GENERAL FEATURES OF PHYTOPLANKTON 17
Figure 1.4 Filamentous
phytoplankters. Filamentous
coenobia of the diatom Aulacoseira
subarctica (a, b; b also shows a
spherical auxospore) and of the
Cyanobacteria (c) Gloeotrichia
echinulata, (d) Planktothrix mougeotii,
(e) Limnothrix redekei (note polar gas
vacuoles), (f) Aphanizomenon
flos-aquae (with one akinete formed
and another differentiating) and
Anabaena flos-aquae (g) in India ink,
to show the extent of mucilage, and
(h) enlarged, to show two
heterocysts and one akinete. Scale
bar, 10 µm. Original
photomicrographs by Dr H. M.
Canter-Lund, reproduced from
Reynolds (1984a).
neutral buoyancy would provide the only ideal
adaptation). However, natural water bodies are
almost never still. Movement is generated as a
consequence of the water being warmed or cool-
ing, causing convection with vertical and hori-
zontal displacements. It is enhanced or modified
by gravitation, by wind stress on the water sur-
face and by the inertia due to the Earth’s rotation
(Coriolis’ force). Major flows are compensated by
return currents at depth and by a wide spectrum
of intermediate eddies of diminishing size and
of progressively smaller scales of turbulent diffu-
sivity, culminating in molecular viscosity (these
motions are characterised in Chapter 2).
To a greater or lesser degree, these move-
ments of the medium overwhelm the sinking tra-
jectories of phytoplankton. The traditional view
of planktic adaptations as mechanisms to slow
sinking rate needs to be adjusted. The essential
requirement of phytoplankton is to maximise the
opportunities for suspension in the various parts
of the eddy spectrum. In many instances, the
adaptations manifestly enhance the entrainabil-
ity of planktic organisms by turbulent eddies.
These include small size and low excess den-
sity (i.e. organismic density is close to that of
water,