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PHYSIOLOGY OF THE CLADOCERA
This page intentionally left blank
PHYSIOLOGY
OF THE
CLADOCERA
SECOND EDITION
Nikolai N. Smirnov
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

With Additional Contributions

Academic Press is an imprint of Elsevier
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(other than as may be noted herein).
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our understanding, changes in research methods, professional practices, or medical treatment may become
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 Contents

List of Contributors ix 5.4 Hemoglobin and Iron 93

5.5 Evolution of Carbon Dioxide and the Respiratory
Preface xi Quotient (RQ) 96
Acknowledgments xiii 5.6 Energy Budget 97
Abbreviations and Units xv 5.7 Hypoxia 97
5.8 Anoxia 99
1. General 5.9 Impact of Xenobiotics on Respiration 100

1.1 Systematic Position 1 6. Circulation

1.2 General Morphological Background 1
1.3 Geographic Distribution 6 6.1 Anatomical Background 101
1.4 Species-Specific Effect of Xenobiotics 7 6.2 Blood Flow 102
6.3 Heart Rate 103
2. Methods 6.4 Heart Regulation 106
6.5 Heart Arrest 109
2.1 Methods of Collection 9 6.6 Adhesion of Blood Cells 110
2.2 Observation of Living Specimens 9 6.7 Phagocytosis 110
2.3 Cultivation 9 6.8 Impact of Xenobiotics on Heart Rate 111
2.4 Immobilization and Attaching 10
2.5 Microscopy 11 7. Excretion
2.6 Biochemical and Special Physiological Methods 11
7.1 Anatomical Background 113
3. Chemical Composition 7.2 The Process of Excretion 114
7.3 Bioaccumulation of Toxic Substances 116
3.1 Lability of Chemical Composition 13 7.4 Transformation of Xenobiotics 118
3.2 Moisture Content and Calorific Value 13 7.5 The Routes of Elimination of Xenobiotics 118
3.3 Principal Constituents 13
3.4 Accumulation of Xenobiotics in the Cladoceran 8. Osmotic Regulation
Body 36
8.1 Potential Anatomical Background 121
4. Nutrition 8.2 Environmental Background 121
8.3 Water Balance 122
4.1 Feeding 39 8.4 Process of Osmotic Regulation 123
4.2 Digestion 60 8.5 Effect of Xenobiotics on Osmotic Regulation 126

5. Respiration 9. Cell and Tissue Metabolism

5.1 Anatomical Background 89 9.1 Enzymes in the Body of Cladocera 127
5.2 Environmental Background 89 9.2 Endocrine and Exocrine Secretion 128
5.3 Oxygen Consumption 90 9.3 Antioxidant System 129

v
vi CONTENTS

9.4 Effects of Toxic Compounds on Cytology and 14. Behavior

Metabolic Factors 131
9.5 Detoxification 135 14.1 Differences in Behavior Among Species 211
14.2 Migration and Swarming 212
10. Growth and Molting 14.3 Emotional Reactions 214
14.4 Impact of Xenobiotics on Behavior 216
10.1 Size and Weight Characteristics 137
10.2 Growth 137 15. Ecophysiology
10.3 Modification of Form 140
10.4 Molting 143 15.1 Physiological Background of the Limits of
10.5 Senescence 146 Environmental Factors 218
10.6 Impact of Xenobiotics 147 15.2 Adaptation 221
15.3 Genotypes 222
11. Reproduction 15.4 Environmental Conditioning by Cladocera 222
15.5 Cladocera in the Polluted Hydrosphere 224
11.1 Anatomical Background 151 15.6 Synergism and Antagonism Among Environmental
11.2 Cyclicity 151 Factors 226
11.3 Parthenogenetic Reproduction 152 15.7 Cladocera as Tools in Water Quality and Medical
11.4 Gamogenetic Reproduction; Diapause 155 Testing 227
11.5 The Physiology of Eggs and Embryos 157
11.6 The Physiology of Males 166 16. A Cytological Perspective
11.7 Sex Hormones 167 MARGARET J. BEATON, CARLI M. PETERS
11.8 Impact of Anthropogenic Factors on
Reproduction 171 16.1 Genome Size and Polyploidy 232
16.2 Cytogenetics 238
12. Locomotion 16.3 Endopolyploidy 241
16.4 Cytological Observations for Specific
12.1 Anatomical Background 175 Tissues 244
12.2 Environmental Background 177 16.5 Reproduction 249
12.3 Movement Trajectories 179 16.6 Concluding Remarks 252
12.4 Muscle Physiology 182
12.5 Immobilization 182
12.6 Fatigue and Stress 183 17. The Genomics of Cladoceran Physiology:
12.7 Impact of Toxicity on Locomotion 184 Daphnia as a Model
K. VAN DAMME, D. BECKER, E. TURNER,
13. Nervous System and Sense Organs J.R. SHAW, J.K. COLBOURNE, B. ZEIS,
M. CORDELLIER, E. DECAESTECKER,
13.1 Anatomical Background: Sense Organs 187 M.E. PFRENDER
13.2 Neurosecretion 189
13.3 Sense Organs 193 17.1 Introduction 253
13.4 Vision 194 17.2 History of Research: The Pregenomics Era 255
13.5 Effects of Electromagnetic Fields 205 17.3 Daphnia as a Model System for Physiological
13.6 Chemoreception 205 Genomics 257
13.7 Mechanoreception 206 17.4 Daphnia’s Ecoresponsive Genome 260
13.8 Endogenous Rhythms of Activity 209 17.5 The Genetic Basis of Physiological Plasticity: A Case
13.9 Effect of Xenobiotics 210 Study 263
 CONTENTS vii
17.6 Hunting for Physiologically Relevant Genes and 18.5 Nervous System and Sensory Organ
Regulatory Networks 268 Formation 290
17.7 Comparing Past to Present Physiologies 273 18.6 Gonad Formation 291
17.8 Future Directions: Exploring Physiological Variation 18.7 Hormonal Regulation of Embryonic
With Functional Genomics 275 Molts 292
Glossary Terms 278 18.8 Kairomones and Embryos 292
18.9 Osmoregulation in Embryos 294
18. Notes on the Physiology of 18.10 Respiration 295
Embryogenesis 18.11 Yolk and Glycogen 296
18.12 Miscellaneous Observations 296
A.A. KOTOV
Conclusions: Special Traits of Cladoceran
18.1 Short History 281
18.2 General Information and Staging 281 Physiology 299
18.3 Earlier Development: Cleavage, Blastulation,
Start of Segmentation, and Start of References 303
Neurogenesis 284 Index of Latin Names of Cladocera 387
18.4 Hox Genes and Expression of Other Genes 286 Subject Index 389
This page intentionally left blank
 List of Contributors

M.J. Beaton Mount Allison University, Sackville, M.E. Pfrender University of Notre Dame, Notre
NB, Canada Dame, IN, United States
D. Becker University of Virginia, Charlottesville, J.R. Shaw Indiana University, Bloomington, IN,
VA, United States United States
J.K. Colbourne University of Birmingham, Birming- N.N. Smirnov A. N. Severtsov Institute of Ecology
ham, United Kingdom and Evolution, Russian Academy of Sciences,
M. Cordellier Universit€at Hamburg, Hamburg, Moscow, Russia
Germany E. Turner Indiana University, Bloomington, IN,
E. Decaestecker KU Leuven Campus Kulak, United States
Kortrijk, Belgium K. Van Damme Senckenberg Research Institute and
A.A. Kotov A. N. Severtsov Institute of Ecology and Museum of Nature, Frankfurt am Main, Germany
Evolution, Russian Academy of Sciences, B. Zeis Muenster University, Muenster, Germany
Moscow, Russia
C.M. Peters University of British Columbia,
Vancouver, BC, Canada

ix
This page intentionally left blank
 Preface

Increasing and universal environmental some issues are now clarified and some are
pollution stimulated numerous recent investiga- almost unknown.
tions in the pathological physiology of the Over 700 species of Cladocera (Crustacea:
Cladocera that brought forth abundant informa- Branchiopoda) are known and representatives
tion discussed in the present edition. In addition, of this group are often dominant in the fresh-
studies in normal physiology progressed in water fauna, sometimes occurring in enormous
various ways. quantities. They live in both small and large wa-
The structure of the previous edition is only ter bodies from arctic to tropical latitudes, in
slightly changed. However, new sections are open water, on the bottom, in mud, among
added and numerous new findings are intro- inshore vegetation, in acid pools on bogs, in
duced throughout the text. As well, misprints small accumulations of water in epiphytic
and errors are corrected. The present edition is plants, in narrow aquatic spaces between moist
supplemented mainly with data from sources sand grains. A few species even left the water
for recent years. and live in moist moss-like growth on tree trunks
Reviewing the results of the worldwide inves- in tropical cloud forests. Some species are
tigations one may note that they remain mostly specialized for life in saline lakes and in the sea.
confined to daphnids which live in open water, Cladocerans, especially Daphnia species,
especially to Daphnia, whereas representatives belong to the commonest animals in hydro-
of other families coping with different life condi- biology. They are counted, measured, weighed,
tions are still awaiting investigation. The vast cultured, their species lists are composed, distri-
and specific world of littoral and bottom-living bution in space and time described. Their role is
Cladocera is still waiting for due physiological recognized as the food resource of fish and as
assessment. Some data available for such species water quality indicators. Species of Cladocera
are discussed as well. Transformations of func- are described and redescribed nowadays in
tions and the related structures in different fam- excellent morphological detail.
ilies would be highly instructive and revealing. Usually, little more is taken into consideration
Probably, the present review will indicate what than a cladoceran as a living object with individ-
and how should further be studied in these ani- ual, mostly external, traits that permit species
mals which live very differently from pelagic recognition. There follows an attempt to summa-
species. Especially demonstrative would be, rize information showing that the Cladocera
e.g., data on transformations of the system of possess complicated and special metabolism
muscles and of the involved skeletal structures and behavior which deserve knowing, as these
performing different kinds of locomotion in rep- data may explain how and why Cladocera spe-
resentatives of various genera. cies successfully live in their various media.
Another special point of studies in Cladocera The following summary is an attempt to
physiology is that they are still fragmentary: contribute to a more profound understanding

xi
xii PREFACE

of how and why they participate in the processes of explanation is supplied by morphology (struc-
developing in inland waters. Particular chapters tural traits), e.g., thin skeletons, swimming ap-
of cladoceran physiology are still covered very pendages, oil drops, sometimes the presence of
unevenly. Recently, numerous and more in- slime, etc., in planktonic forms. However, phys-
depth data on pathological physiology are being iology makes a wide field which can be used for
accumulated, comparing with older data that understanding causative relationships.
were confined mostly to longevity and amount Daphnia is more and more frequently used in
of progeny as affected by xenobiotics. water-quality testing and as a model organism
Comparative physiological investigations of supposed to represent situations in natural or
representatives of various families with their artificial ecosystems (Lampert, 2011; Seda and
different ecology are urgently desirable and Petrusek, 2011).
would make a promising field. Of course, some- Along with special discussions, introductory
times more questions are raised than answers remarks are made whenever it seemed to be
supplied. The present review of this vast field necessary to make the matter useful both for spe-
is rather an attempt at systematic assembling cialists and for nonspecialists.
of the available data and demonstration of spec- The present review comprises studies made in
ificity of this group of crustaceans. Within the the period starting from the second half of
present context, the main attention is paid to the 19th century. Completeness of information
data demonstrating which and how the meta- was checked against Zoological Record, part
bolic links are influenced by particular natural 10 (Crustacea), vols 1e150 (for 2015) and
and anthropogenic factors in the hope of Russian Referativnyi Zhurnal (Biology, Zoology)
revealing the reasons of this impact. (1992e2015). Some earlier sources are also
Investigations of aquatic invertebrates added. Any incompleteness herein is because
frequently endeavor to obtain answers why a some fields are not yet investigated, some litera-
certain species is present or absent, why it is ture has not been found, and some points might
abundant, why it lives in a certain habitat. Part have escaped the author’s attention.
 Acknowledgments

The present volume is an attempt at making a sufficient for direct understanding of original
summary of work of many experts throughout texts. Many librarians, mostly personally un-
the world in various fields using special known to the author, retrieved numerous publi-
methods. A substantial contribution to physi- cations in different languages and times. Their
ology of the Cladocera has recently been made care and labor are appreciated, including those
by toxicologists. of Ms. N.I. Gotovskaya and Ms. E.V. Morozova
Special thanks are due to Dr. M.J. Burgis the Biological Department Library of the Russian
(United Kingdom) who generously used her Academy of Sciences (RAS). The facilities and
time and experience to make the manuscript of library of the Moscow Society of Naturalists
the first edition acceptable. were very useful, especially for earlier sources.
The present review is motivated by the Dr. V.R. Alekseev and Ms. N.M. Sukhikh were
author’s observations on living, mostly littoral, very helpful in work with resources of the li-
cladocerans. Both the initial training and subse- brary of the Zoological Institute RAS (St. Peters-
quent work of the author implied that hydrobiol- burg). I am sincerely grateful to Professor G.A.
ogy is impossible without physiological data. Boxshall (FRS; UK) for help in getting rare
Some recent observations are made at the publications.
Hydrobiological Station “Lake Glubokoe” My wife, L.A. Smirnova, Ph.D. (cited here as
(Russia). The author is grateful to his immediate L.A. Luferova) is tolerant (mostly) toward using
colleagues from the “Cladocera team” for help a big part of my time for such ventures as this.
and discussions: O.S. Boikova, N.M. Korovchin- Formulation of ideas included in this book
sky, A.A. Kotov, E.I. Bekker, and A.Y. Sinev. and its composition was much favored by
Dr. Kotov critically read the draft manuscript, creative environment at the Institute of Ecology
suggested numerous useful additions, and used and Evolution of the RAS, and by personal atten-
his skill for preparation of the manuscript and tion of academicians D.S. Pavlov and Yu.Yu.
figures. Dgebuadze.
The author is obliged to many teachers at The authors of Chapters 16e18 described
school and at the Linguistic University their special fields and made the subject much
(Moscow) for training in European languages more advanced and complete.

xiii
This page intentionally left blank
 Abbreviations and Units

Standard abbreviations and units are used.

ACh Acetylcholine
ATP Adenosine triphosphate
DHA Docosahexaenoic acid
DNA Deoxyribonucleic acid
DW Dry weight
EPA Eicosapentaenoic acid
FAs Fatty acids
GST Glutathione S-transferase
h Hour
Hb Hemoglobin
HUFAs Highly unsaturated fatty acids
IUs International units
MF Methyl farnesoate
mg% mg per 100 g
min Minute
MUFAs Monounsaturated fatty acids
NADH Nicotinamide adenine dinucleotide plus hydrogen
PCBs Polychlorinated biphenyls
PUFAs Polyunsaturated fatty acids
RNA Ribonucleic acid
RQ Respiratory Quotient
SAFAs Saturated fatty acids
TBT Tributyltin chloride
UVR Ultraviolet radiation
WW Wet weight

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