Meiobenthology The Microscopic Motile Fauna of Aquatic Sediments pot

par-His review The Interstitial Fauna of Marine Sand 1964 is considered a classic among early meiofaunal literature.. Working along the shores of the Mediterranean Sea, Delamare Deboutt

The Microscopic Motile Fauna

of Aquatic Sediments

The Microscopic Motile Fauna

of Aquatic Sediments

2nd revised and extended edition with

125 Figures, 20 Tables, and 41 Information Boxes

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Cover illustration: Two interstitial Amblyosyllis (Annelida: Syllidae); courtesy of Nathan W Riser,

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to whom I owe it all

Also bestimmt die Gestalt die Lebensweise des Thieres, und die Weise zu leben sie wirkt auf alle Gestalten mächtig zurück.

So the shape of an animal patterns its manner of living, likewise their manner of living exerts on the animals’ shape

goethe 1806: Metamorphose der Thiere

Encouraged by the friendly acceptance of the first edition and stimulated by numerous requests and comments from the community of meiobenthologists, this second edition updates my monograph on meiobenthology The revised text emphasizes new discoveries and developments of relevance; it has been extended by adding chapters on meiofauna in areas not covered before, such as the polar regions, mangroves, and hydrothermal vents As I attempted to keep

up with the actual literature for the whole field of meio benthos—taxonomy and ecology, marine and freshwater—I became a little discouraged upon noticing the flood of literature that had appeared in the few years after the publication

of the first edition Has there been a multiplication of new meiobenthologists or

an inflation of their industrious efforts? How could I compile this plethora of new data; how to select, what to omit? The need to extract general information from the details, and to modify and amalgamate them within a greater context; this difficult “condensation” process was the key to my approach It forced me

to be selective, to focus on one goal: to write a readable compendium that will serve the interested biologist, the fellow benthologist and the student alike Avoiding a style with constructions that are too sophisticated should also enhance the comprehension of those readers that are not natively familiar with the English language

Since the first edition, meiofaunal research has made, I believe, major progress in three general areas: (a) systematics, diversity, and distribution; (b) ecology, food webs

vii

and energy flow; and (c) environmental aspects, including studies of anthropogenic impacts.

(a) In the area of systematics, diversity and distribution, molecular biological studies suggest that some of the “smaller” meiobenthic groups, such as Kinorhyncha, Gastrotricha and Rotifera, hold key positions in metazoan phy-logeny, linking various invertebrate lines into new units (e.g., Ecdysozoa, Scalidophora, Cycloneuralia, Lophotrochozoa) Genetic fine-scale diversifi-cation has become an indispensable tool for understanding distribution processes and biogeographic patterns With enhanced studies in exotic and remote areas, the meio benthos continues to be a haven for the discovery of unknown animals, even of high taxonomic rank, e.g., Micrognathozoa Reports on meiofauna from polar or tropical regions, deep-sea bottoms or hydrothermal vents were limited in the first edition due to the scarcity of per-tinent studies Recent comprehensive publications have now recognized these formerly exotic areas as being in the research mainstream, and are covered here in separate chapters Problems of principal biological relevance, such as the study of distribution patterns or the relation of body size to distribution, have been tackled using meiofauna as tools The high number of meiobenthic species found under even extreme or impoverished ecological conditions puts meio benthos at the forefront of biodiversity and “census of life” studies Taxonomic, functional and genetic diversity as influenced by ecological and/

or anthropogenic variables are widely acknowledged matters of concern Molecular screening methods allow large numbers of species to be recorded upon expending reasonable effort

(b) Today, essays on aquatic environments mostly consider the relevant role of benthos Mucus agglutinations and microorganisms are increasingly recognized to

meio-be important components that structure the sediment texture and provide the basis for many meiobenthic food chains Trophic fluxes can be followed using new techniques, such as by assessing isotopic signatures Metabolic pathways visualized by fluorescence imaging enable us to broaden our limited knowledge

of the physiology of meio benthos Combined with advanced statistics, such as multivariate analyses, we can achieve results that link meio benthos to general ecological paradigms

(c) The reactions of biota to environmental threats are increasingly based on ations of the meiofauna, underlining their inherent advantages (small size, ubi-quity, abundance) With improved processing and culturing methods, pollution experiments are now often based on meiobenthic animals, apply population dynamics and use micro-/mesocosm studies Standardized bioassays include meiofauna and have become commercially available The increased role of meiofauna in this field is reflected by new chapters on the impact of metal com-pounds and pesticides The use of molecular techniques can alleviate the prob-lem of rapid mass identification, e.g., in nematodes

evalu-All of these research fields tie meiobenthology closer to the “mainstream,” which should be a main goal of future meiobenthic research If this second edition can

synthesize these modern scientific achievements, meiobenthology could indeed play a key role in assessing the health of our environment, and will not just represent

a playground for singular interests

Several comprehensive publications on meio benthos published in the last few years are contributing to this goal Of broad interest are monographic publications

on freshwater meio benthos (Hakenkamp and Palmer 2000; Hakenkamp et al 2002; Robertson et al 2000a; Rundle et al 2002) The new edition of the classic treatise

Methods for the Study of Marine Benthos (Eleftheriou and McIntyre 2005) contains competent contributions to sediment analysis, sampling strategies and meiofauna techniques (Somerfield et al 2005) It also covers statistical and analytical methods that assess ecosystem functioning and measure energy flow through benthic populations

Therefore, in this edition of Meiobenthology I have condensed the information in

some chapters referring to “Methods for the Study of Marine Benthos.” Lesser known are the meiofauna reviews of Galhano (1970, in Portuguese) and Gal’tsova (1991, in Russian), which were not mentioned in the first edition In other chapters

of this edition (e.g., on polluted sites), the scope has been expanded by adding short accounts of the impacts of metals and pesticides on meio benthos The most conspicuous novelty is the highlighted boxes, which either contain the essence of a particular section or comment on special aspects

The figures have been redesigned for higher clarity, and some outdated paragraphs have been shortened or omitted To maximize readability not all of the publications

on which I drew are cited; on the other hand, on several occasions the same tion is cited in a different context in order to make the chapters independently reada-ble and understandable The resulting reference list is meant to provide an archive of detailed studies in all fields of meiobenthology A comprehensive index and a glos-sary explaining specific terms facilitate the use of this book Because of their ease of accessibility for the general reader, I accentuate references in widely distributed, English-dominated journals As much as all this may help to improve the distribution and didactic impact of this book, I especially hope, for the sake of the student reader, that Springer-Verlag publishes this new edition at a competitive price that is afforda-ble to all interested in the great world of small organisms I hope that this edition will

publica-be considered as readable and received as warmly by the readers as the 1993 edition

Despite all the care that I have taken, I could not consider every contribution, and

so I apologize especially to those colleagues who have published in less common native languages or in journals with restricted distributions, whose results have not been con-sidered here My particular regrets remain realizing how much valuable knowledge is

“hidden” to most of us in the numerous publications that have appeared in Russian over the last few years, much of it unnoticed by many of us Mistakes in the first edi-tion, for which I apologize, have hopefully been eliminated I regret and take the responsibility for remaining omissions or erroneous interpretations

Should this book draw the attention of benthic ecologists to the relevance of meio benthos and foster further research in this field, it has accomplished its goals Perhaps it represents the last chance to write a monographic textbook that amalga-mates bits of information into a coherent context before electronic databases,

pictures and information networks produce a glut of innumerable details and lications—an information jungle in which the beginner especially can easily become lost.

pub-Meiobenthology is now increasingly represented on the Internet: the International Association of Meiobenthologists (I.A.M.) and also many colleagues have often designed comprehensive homepages with address and publication lists New editions

of the I.A.M newsletter Psammonalia are regularly published online (http://www.

meiofauna.org/) and include pictures and even short movie galleries Also, CD-ROMs and databases of computer-based pictorial identification keys have attained increasing importance (European Limnofauna; European Register of Marine Species, ERMS; separate databases for Nematoda, Harpacticoida, Turbellaria)

With this book I conclude many of my activities in meiobenthology To express my feelings I could do worse than adopting the words of a good friend and protagonist of meio benthos research, Prof Bruce C Coull, who upon his retirement wonderfully characterized his feelings and probably those of many other fellow meiobenthologists

of our peer group: “I maintain an interest in all things meiofaunal and it has been a great life studying them I hope that the next generation of researchers will learn much more about these creature friends and that the researchers have as much fun as I have had trying

to understand our ubiquitous and omnipresent aquatic denizens.”

Acknowledgements The second edition has been carefully proof-read again by my friend Robert

P Higgins (Ashville, NC, USA) His dedication and encouragement constantly accompanied me while writing this text Important chapters have been kindly reviewed by two other good friends and experts, Bruce C Coull (Columbia, SC, USA) and Walter Traunspurger (Bielefeld, Germany)

I owe a large intellectual debt to all those many colleagues who invaluably helped me by sending literature, giving comments and, most importantly, kept encouraging me to complete this work There are far too many to mention them all here by name I thank Mrs M Hänel for her detailed drawings and particularly Mrs A Kröger (both Hamburg) for her most valuable and patient com- puter skills when designing the figures Finally, Springer-Verlag (Heidelberg, Berlin) is to be thanked for its continuous interest in this project and its “author-friendly” support throughout the correspondence.

Studies on meio benthos, the motile microscopic fauna of aquatic sediments, are gaining in importance, revealing trophic cycles and allowing the impacts of anthro-pogenic factors to be assessed The bottom of the sea, the banks of rivers and the shores of lakes contain higher concentrations of nutrients, more microorganisms and a richer fauna than the water column Calculations on the role of benthic organisms reveal that the “small food web”, i.e., microorganisms, protozoans, microphytob-enthos, and smaller metazoans, play a dominant role in the turnover of organic matter (Kuipers et al 1981) New animal groups—even those of high taxonomic status—are often of meiobenthic size and continue to be described Two of the most recent animal groups ranked as phyla, the Gnathostomulida and the Loricifera, represent typical meio benthos.

Up to now, a textbook introducing the microscopic organisms of the sediments, their ecological demands and biological properties has not existed, despite the sig-

nificance of meio benthos indicated above A recent book entitled Introduction to the Study of Meiofauna (Higgins and Thiel 1988) gives valuable outlines for practi-

cal investigation, and Stygofauna Mundi, a monograph edited by Botosaneanu

(1986a), focuses on zoogeographical aspects of mainly freshwater forms, but ther was intended to be a comprehensive text on the subject of meiobenthology.The purpose of this book is to provide a general overview of the framework and the theoretical background of the scientific field of meiobenthology The first of three major parts describes the habitat of meio benthos and some of the methods used for its investigation; the second part deals with morphological and systematic aspects of meiofauna, and the third part reports on the meiofauna of selected biotopes and on community and synecological aspects of meio benthos However, a monographic text cannot include an adequate survey of general benthic ecology, or be a textbook on the zoology of microscopic animal groups The primary purpose of this text is to provide

nei-an ecologically oriented scientific basis for meiobenthic studies Further advice for practical investigations is found in important compilations by Higgins and Thiel (1988), Holme and McIntyre (1984), and Gray (1981) Hence, aspects of sampling procedures and strategies, statistical treatment and fauna processing will be treated here only briefly In these fields, the present work should be considered a supplement

to the books mentioned above and instead focuses on some critical hints, logical limitations, and a few neglected practical aspects

methodo-xi

Writing this book was particularly difficult because the literature on meiofauna

is so widely dispersed in journals and congress proceedings and has so rapidly increased in volume that complete coverage is impossible Regardless of my efforts, therefore, there is no pretence that this text is absolutely comprehensive Where it is important for the general context, the major chapters of the book contain some overlap in terms of information This is deliberate; it provides the reader with chapters that are complete in themselves and avoids the need for too many cross-references Also, in order to maintain a readable, coherent style, citations of spe-cific references had to be restricted Thus, the “reference list” of this text does not represent all of the sources drawn upon during the production of this book.The selection of topics and the emphasis given to them is admittedly subjective

In particular, the brief treatment of freshwater meio benthos (Chapter 8.2) by no means reflects the exhaustive achievements and importance of this field of meiob-enthology This book does not include the nanobenthos, since this represents a microbiota that is completely different from the meio benthos in its size range, methodology, and taxonomical composition (mainly prokaryotes, often autotrophic protists and fungi) Where appropriate, references compiled in a “Recommended reading” paragraph are given at the ends of many chapters They will serve as sup-plementary information and, hopefully, will compensate for my own subjectivity Should incorrect or misunderstood data be reported in the text, I would be most grateful to be informed of this

This book resulted from a series of lectures for advanced students given by the author over a period of several years at the University of Hamburg Studying the tiny organisms living in sand and mud fascinated many of the students and provided the encouragement and persistent stimulus needed to write this book It will achieve its goal if it further promotes interest in the diverse and cryptic microscopic world of meiobenthic animals, emphasizes their ecological importance, from both theoretical and practical viewpoints, and contributes to the awareness that small animals often play a key role in large ecosystems, which are becoming increasingly threatened

Acknowledgements I am deeply obliged to Dr Robert P Higgins (Washington, DC), who cally reviewed the entire text, and not only for linguistic flaws My thanks go out to my graduate students who supported me in selecting figures and designing graphs I am grateful to several of

criti-my colleagues for their valuable comments on parts of the text, and for providing me with scripts that were sometimes still in press and for other helpful hints It was my intention to include only originals or redrawn figures This was possible through the patient work of A Mantel and M Hänel (both in Hamburg), for which I am most grateful.

1 Introduction to Meiobenthology 1

1.1 Meiobenthos and Meiofauna: Definitions 1

1.2 A History of Meiobenthology 2

2 The Biotope: Factors and Study Methods 7

2.1 Abiotic Factors (Sediment Physiography) 7

2.1.1 Sediment Pores and Particles 7

2.1.2 Granulometric Characteristics 9

2.1.3 The Sediment–Water Regime 14

2.1.4 Physicochemical Characteristics 22

2.2 Biotic Habitat Factors: A Connected Complex 37

2.2.1 Detritus and Particulate Organic Matter (POM) 38

2.2.2 Dissolved Organic Matter (DOM) 40

2.2.3 Mucus, Exopolymers, and Biofilms 41

2.2.4 Bacteria 43

2.2.5 Microphytobenthos 48

2.2.6 Higher Plants 53

2.2.7 Animals Structuring the Ecosystem 53

2.3 Conclusion: The Microtexture of Natural Sediments 59

3 Sampling and Processing Meiofauna 63

3.1 Sampling 63

3.1.1 Number of Replicates and Size of Sampling Units 63

3.1.2 Sampling Devices 64

3.2 Processing of Meiofaunal Samples 72

3.2.1 Preserving Meiofauna in Their Natural Void System 72

3.2.2 Extraction of Meiofauna 73

3.2.3 Fixation and Preservation 77

3.2.4 Processing and Identifying Meiofaunal Organisms 80

3.3 Extraction of Pore Water 84

xiii

4 Biological Characteristics of Meiofauna 87

4.1 Adaptations to the Biotope 87

4.1.1 Adaptations to Narrow Spaces: Miniaturization, Elongation, Flexibility 87

4.1.2 Adaptations to the Mobile Environment: Adhesion, Special Locomotion, Reinforcing Structures 92

4.1.3 Adaptations to the Three-Dimensional Dark Environment: Static Organs, Reduction of Pigment and Eyes 97

4.1.4 Adaptations Related to Reproduction and Development 99

5 Meiofauna Taxa: A Systematic Account 103

5.1 Protista (Protoctista) 103

5.1.1 Foraminifera (Rhizaria: Granuloreticulosa) 103

5.1.2 Heliozoa (Actinopodia) 107

5.1.3 Amoebozoa (“Rhizopoda”): Gymnamoebea, Testacea 107

5.1.4 Ciliophora (Ciliata) 108

5.2 Cnidaria 114

5.2.1 Hydroida (Medusae) 116

5.2.2 Hydroida (Polyps) 116

5.2.3 Scyphozoa 118

5.2.4 Anthozoa 118

5.3 Free-Living Platyhelminthes: Turbellarians 119

5.3.1 Major Turbellarian Groups 120

5.3.2 Distributional and Ecological Aspects 123

5.4 Gnathifera 127

5.4.1 Gnathostomulida 127

5.4.2 Rotifera, Rotatoria 129

5.4.3 Micrognathozoa 133

5.5 Nemertinea 134

5.6 Nemathelminthes: A Valid Taxon? 136

5.6.1 Nematoda (Free-Living) 137

5.6.2 Kinorhyncha 156

5.6.3 Priapulida 158

5.6.4 Loricifera 160

5.6.5 Gastrotricha 162

5.7 Tardigrada 165

5.8 Crustacea 171

5.8.1 Cephalocarida 172

5.8.2 Anostraca: Anomopoda (“Cladocera”; “Branchiopoda”) 173

5.8.3 Ostracoda 175

5.8.4 Mystacocarida 180

5.8.5 Copepoda: Harpacticoida 181

5.8.6 Copepoda: Cyclopoida and Siphonostomatoida 189

5.8.7 Malacostraca 190

5.9 Chelicerata: Acari 201

5.9.1 Halacaroidea: Halacaridae 201

5.9.2 Freshwater Mites: “Hydrachnidia,” Stygothrombiidae, and Others 205

5.9.3 Palpigradi (Arachnida) 205

5.9.4 Pycnogonida, Pantopoda 206

5.10 Terrigenous Arthropoda (Thalassobionts) 207

5.11 Annelida 207

5.11.1 Polychaeta 208

5.11.2 Oligochaeta 215

5.11.3 Annelida “Incertae sedis” 218

5.12 Sipuncula 221

5.13 Mollusca 223

5.13.1 Monoplacophora and Aplacophora 223

5.13.2 Gastropoda 225

5.14 Tentaculata 226

5.14.1 Brachiopoda 226

5.14.2 Bryozoa, Ectoprocta 227

5.15 Kamptozoa, Entoprocta 228

5.16 Echinodermata 229

5.16.1 Holothuroidea 229

5.17 Chaetognatha 230

5.18 Tunicata (Chordata) 231

5.18.1 Ascidiacea 231

5.18.2 Sorberacea 232

5.19 Meiofaunal Taxa: Concluding Remarks 233

6 Evolutionary and Phylogenetic Effects in Meiobenthology 235

6.1 Body Structures of Evolutionary Relevance 235

6.2 Meiofauna in the Fossil Record 239

7 Patterns of Meiofauna Distribution 243

7.1 Evolutionary Aspects 243

7.2 Zoogeographic Aspects 249

7.2.1 Mechanisms of Dispersal 250

7.2.2 Geological Structures and Processes 256

7.3 Ecological Aspects of Distributional Importance: Horizontal Patterns 259

7.4 Vertical Zonation of Meio benthos 261

8 Meiofauna from Selected Biotopes and Regions 267

8.1 Polar Regions 268

8.1.1 Sea Ice 270

8.2 Marine Subtropical and Tropical Regions 276

8.2.1 Tropical Sands 278

8.2.2 Mangroves 280

8.3 The Deep-Sea 284

8.3.1 The Habitat 284

8.3.2 The Meiofauna 287

8.4 Dysoxic, Anoxic, and Sulfidic Environments: Discussing the Thiobios 296

8.4.1 Reducing Habitats of the Thiobios 296

8.4.2 Thiobiotic Meio benthos 298

8.4.3 Survival of Thiobios Under Anoxia and Sulphide – Mechanisms and Adaptations 302

8.4.4 Food Spectrum of the Thiobios 307

8.4.5 Distribution and Succession of the Thiobios 308

8.4.6 Diversity and Evolution of the Thiobios 309

8.4.7 Chemoautotrophy-Based Ecosystems: Vents, Seeps, and Other Exotic Habitats 313

8.5 Phytal Habitats and Hard Substrates 317

8.6 Brackish Water Sites 324

8.7 Freshwater Biotopes 328

8.7.1 Running Waters: Stream and River Beds 329

8.7.2 The Groundwater System 338

8.7.3 Standing Waters, Lakes 344

8.8 Polluted Habitats 349

8.8.1 General Aspects and Method Survey 349

8.8.2 Selected Cases of Pollution and Meiofauna 361

9 Synecological Perspectives in Meiobenthology 373

9.1 Community Structure and Diversity 373

9.1.1 Processes of Recolonization 375

9.2 Community Structure and Size Spectra 377

9.3 The Meio benthos in the Benthic Energy Flow 383

9.3.1 General Considerations 383

9.3.2 Assessing Production: Abundance, Biomass, P/B Ratio, Respiration 387

9.3.3 The Energetic Divergence Between Meiofauna and Macrofauna 397

9.4 The Position of Meiofauna in the Benthic Ecosystem: A Compilation of Energy Fluxes 400

9.4.1 The Meiofauna as Members of the “Small Food Web” 402

9.4.2 Links Between the Meiofauna and the Macrofauna 406

9.4.3 Meiofauna as an Integrative Benthic Complex 410

10 Retrospect on Meiobenthology and Outlook

on New Approaches and Future Research 417

References 423

Glossary 503

Index 513

Introduction to Meiobenthology

1.1 Meio benthos and Meiofauna: Definitions

The terms “macrobenthos” and “microbenthos” were already well established when

in 1942 Molly F Mare coined the term “meio benthos” to define an assemblage of benthic metazoans that can be distinguished from macrobenthos by their small sizes (note that the Greek “µειος” means “smaller”) Therefore, the study of meio-benthos per se is a relatively new component of benthic research, despite the fact that meiobenthic animals have been known about since the early days of micros-copy This book will mainly focus on metazoan meiofauna, which mirrors the author’s field of expertise Hence, the term “meio benthos” is used here synony-mously to “meiofauna.” However, an ecological picture cannot be drawn without also considering relevant benthic protists (e.g., ciliates, foraminiferans, amoebo-zoans), and microalgae (e.g., diatoms)

Today, members of the meiofauna are considered mobile and sometimes also haptosessile benthic animals, smaller than macrofauna but larger than microfauna (the latter term is now restricted mostly to Protozoa) The formal size boundaries

of meiofauna are operationally defined, based on the standardized mesh width of sieves with 500 µm (1,000 µm) as upper and 44 µm (63 µm) as lower limits: all fauna that pass through the coarse sieve but are retained by the finer sieve during sieving are considered meiofauna In a recent move, a lower size limit of 31 µm has been suggested by deep-sea meiobenthologists in order to quantitatively retain even the smallest meiofaunal organisms (mainly nematodes) Using biomass as a meas-ure, meiofauna (in freshwater) have been defined to include all mobile benthic organisms with masses of between 2 and 20 µg (Hakenkamp et al 2002) What began as an arbitrarily defined size-range of benthic invertebrates has since been supported by studies on the size spectra of marine benthic fauna Quantitative size-taxon studies (Schwinghamer 1981a; Warwick 1984; Warwick et al 1986a; Duplisea and Hargrave 1996—see Sect 9.2) infer that the (marine) meiofauna represent a separate biologically and ecologically defined group of animals, a concept well known in the case of the (interstitial) meiofauna of sands (Remane 1933, see Sect 1.2)

In addition to the “permanent” meiofauna, members of the “temporary” meiofauna belong to the meiofaunal size category only as newly settled larvae that later grow

© Springer-Verlag Berlin Heidelberg 2009

to become macrofauna An exact upper size limit that will be passed by these temporarily small organisms (often juvenile molluscs and annelids) is difficult to define.

Meiofauna are mostly found in and on soft sediments, but also on and among epilithic plants and other hard substrates (e.g., animal tubes) Even the surfaces of barren rocks with their biofilm and detritus cover are suitable habitats Under each footprint of moist shore sediment we often find 50,000–100,000 meiobenthic ani-mals! Indeed, it is unclear why the meio benthos was not recognized earlier as a valid intermediate between the micro- and the macrobenthos It seems inconsistent with the fact that the microscopic fauna in the water column had long been considered

an established faunistic assemblage Personally, I believe that bare sand bottoms and beaches and the often odiferous muds were considered unlikely habitats for diverse fauna of minute dimensions

More detailed reading: Warwick (1989), Palmer et al (2006), Rundle et al (2002)

The term “meiofauna” denotes microscopically small, motile aquatic animals living mostly in and on soft substrates at all depths in the marine and fresh-water realm Although originally restricted to small metazoans, ecological connections suggest that larger protozoans (ciliates, amoebozoans) should also be included in the scope of meiofauna In the context of this book, this wider defi nition is used synonymously with meio benthos Formally defi ned

by sieve mesh sizes of between 44 and 500 mm, meio benthos is increasingly considered an ecological unit of its own, an important link between micro- and macrobenthos In contrast to permanent meio benthos, the newly settled larvae of many macrobenthic animals are temporary meiofauna

1.2 A History of Meiobenthology

Taxonomic descriptions and biological investigations of minute benthic animals were being published by the mid nineteenth century One of the first of these was on

the discovery of a minute aberrant mollusc, the aplacophoran Chaetoderma by

Lovén in 1844, then described as a new worm genus, and the Kinorhyncha described

by Dujardin in 1851 In 1901, Kovalevsky studied Microhedylidae (Gastropoda) in the Eastern Mediterranean, and in 1904, Giard described the first archiannelid

Protodrilus from the coast of Normandy He even stated that the microscopic fauna were so rich “that it would take years to study them.” However, these pioneers of meiofauna considered only isolated taxa—often the exceptional species of known invertebrate groups—not their ecological niches and community aspects

Since then, field investigations were biased towards commercially interesting macrofauna Consequently, a suitable methodology for specifically sampling the smaller benthic animals had to be developed It was Remane who first used fine-meshed plankton nets to filter the “coastal ground water,” and he used dredges with sacks of fine gauze to perform equally pioneering studies of the microscopic fauna

of (eulittoral) muddy bottoms (“pelos”) and of the small organisms associated with surfaces of aquatic plants (“phyton”) ) Remane summarized this work in a mono-

graph entitled Verteilung und Organisation der benthonischen Mikrofauna der Kieler Bucht (1933), where he first used the word “Sandlückenfauna.” The corre-

sponding term “interstitial fauna,” introduced by Nicholls (1935), comprised all animals living in interstices, not only those of meiobenthic size, e.g, polychaetes

in a pebble beach Aside from his important descriptions of new kinds of animals, the significance of Remane’s work is reflected by his contention that the meioben-thic fauna of sand were not merely a loose aggregation of isolated forms, but

“a biocoenosis different not only in species number and occurrence, but also in characteristics of form and function” (Figs 8.11 and 8.12) In his 1952 paper, Remane embodied this concept in the word “Lebensformtypus,” which has since been incorporated into the terminology of general ecology The ubiquity and complexity

of this smaller benthos became much clearer with the development of effective grabs (Petersen 1913) and dredges (Mortensen 1925) for sampling subtidal bottoms.With improved methods (e.g., Moore and Neill 1930; Krogh and Spärck 1936), studies on the small benthos soon emerged from many parts of the world From Remane’s school came numerous German scientists of considerable influence in meiofaunal research, e.g., Ax, Gerlach, Noodt, to name just a few Through their work Remane’s stimulus even proliferated to further generations of meiobentholo-gists (Westheide, Schminke, Riemann) in Germany From Britain, Moore (1930, 1931), Nicholls (1935) and Mare (1942) initiated the study of meiofauna At the beginning of the 1960s Boaden and Gray were among the first to perform experi-ments with marine meiofauna In 1969, McIntyre compiled the first review,

Ecology of Marine Meio benthos, which is still a valuable source of information, ticularly for data on meiofauna from tropical areas By studying the fauna of the Normandy coast of the Channel, the Swedish researcher Swedmark focused atten-tion on the rich interstitial fauna, and described many hitherto unknown species

par-His review The Interstitial Fauna of Marine Sand (1964) is considered a classic

among early meiofaunal literature Working along the shores of the Mediterranean Sea, Delamare Deboutteville concentrated his research into the meio benthos on the brackish transition areas between the marine and freshwater realms He was the

first to conduct meiofaunal research along the African shores His book Biologie des Eaux Souterraines Littorales et Continentales (1960) is another much-esteemed compendium of meiofaunal research

What about North America, now one of the main centers of meiofaunal research? The early marine meiofaunal studies were linked to just a few names, e.g., Pennak, Sanders, and Zinn, who discovered important new crustacean groups Some European scientists working in the US also contributed to the further development

of this field: the studies of the Austrians Riedl, Wieser and Rieger in the 1950–1980s

stimulated several American students to become meiobenthologists The 1960s saw the beginning of American investigations directed primarily at ecology (e.g., Tietjen), which continue to be a major thrust of American meiobenthology, and are mostly concentrated along the Atlantic and Gulf coasts of the United States Beginning in the 1970s the school of Coull began investigating the soft-bottom meiofauna, often addressing environmental problems (disturbance, predation, pollution) and using field experimental methods in estuarine soft bottoms Its impact drew the attention of general marine benthologists to meiofauna.

The development of meiobenthology in the freshwater realm went separate ways, used different methods, and even produced a separate nomenclature Still now, research on freshwater meio benthos is not well coupled with its marine coun-terpart, although both Remane and Delamare Deboutteville often emphasized the connections between marine and freshwater meiofauna, especially those of a zoogeographical and evolutionary nature Similar to the situation in the marine field, important taxonomic work was performed early in the nineteenth century, especially on benthic freshwater copepods (e.g., the works of Sars, Claus, Lang, Gurney), but freshwater meiobenthology, as an ecological discipline, started later

It developed independently with the Russian Sassuchin and colleagues (1927), who sampled at a river shore They first described the “psammon,” i.e., the fauna and flora of sand Today, this term is specified as “mesopsammon,” the fauna between sand grains (= interstitial fauna of sands), in contrast to the mostly macrobenthic

“epipsammon” (i.e., species that live burrowing in the sand) and “endopsammon” (species that live burroweing in the sand) Wiszniewski (1934) conducted similar studies in Polish rivers and lakes that emphasized the important role of rotifers (see Sect 8.7)

While in England, Germany, France and Belgium early papers on the freshwater psammon remained rather isolated and mainly taxonomic in nature, it was the American Pennak who included a wider faunal spectrum in his ecological and

faunistic considerations His monograph Ecology of the Microscopic Metazoa Inhabiting the Sandy Beaches of Some Wisconsin Lakes (1940) is one of the classic publications in freshwater meiobenthology His ecological comparison of freshwater and marine interstitial fauna (1951) provided valuable insights into the characteristics

of these two biomes, an approach later continued in the USA by Palmer and Strayer

Related to the research of Delamare Deboutteville were the investigations of Angelier (1953) on the river shores and banks in the south of France exposed during the dry season Detailed granulometric and physiographic descriptions of the biotopes are a characteristic of this work The importance of the hydrological regime was the subject of the meio benthos studies by Ruttner-Kolisko (beginning

in 1953) in Austrian mountain streams and rivers

In Switzerland Chappuis started a series of investigations (beginning in 1942) on the fauna of the groundwater He found the “stygobios” to be a distinct faunal element (see Sect 8.2.1) The “hyporheic” biotopes beneath streams and rivers were the research domain of Karaman (1935), Orghidan (1955) and collaborators They were attracted by the interesting subterranean fauna of karstic rivers in

Southeast Europe and contributed much to the early knowledge of cave benthos, today also termed “troglobitic” fauna From the 1960s Danielopol worked intensively on hyporheic and lacustrine meio benthos, mainly in Austria Although specializing in ostracods, he and his colleague Stock from Holland also focused on general evolutionary aspects, discussing the colonization pathways for subterra-nean habitats (see Sect 8.7.2).

meio-The ecology of groundwater fauna has been well covered in a volume edited by Gibert et al (1994) A summary of methods for studying freshwater meiofauna has been provided by Palmer et al (2006) Based mainly on lake meiofauna, Rundle

et al (2002) provided a competent review of freshwater meio benthos Meiofauna

of lotic ecosystems (streams) is covered in a special volume edited by Robertson et al (2000a,c) Enhancing our insight into their similarities and differences will hope-fully reduce the historical separation between marine and freshwater meiofaunal research

Today, several hundred scientists are working to expand our knowledge of meiofauna from alpine lakes to the deep-sea floor, from tropical reefs to polar sea ice However, despite an increasing number of meiobenthologists working in Africa, South America, Asia and Australia, the meio benthos in these continents is

as yet largely unknown Studies of the deep-sea meio benthos gain increasing momentum with the development of sophisticated maneuverable vehicles

As in other biological sciences, the structure of meiobenthological research evolved from isolated and individualistic taxonomic descriptions to assessments of abundance and distribution principles worked out by teams These were the founda-tion for ecological research that, after implementing sophisticated statistical methods, could tackle complex problems such as pathways of distribution, community functioning and the impact of disturbances From there, studies on environmental effects and on anthropogenic disturbance and pollution using meiofauna as sentinels were a logical consequence The future of meiobenthology (see Chap 10) will largely depend on how well we understand how to incorporate the specific poten-tials of meiobenthic animals into mainstream benthic research The adoption of molecular methods will decisively contribute to future development We should address the importance of global climate change and advocate more strongly than before the value of using the ubiquitous and speciose meiofauna to assess the health

of ecosystems

Most meiobenthologists are members of the International Association of Meiobenthologists (IAM) (http://www.meiofauna.org/) and thus receive its news-

letter Psammonalia for information on current fields of interest, members’ research

projects and recent literature The triennial conferences of the IAM are important occasions for the mutual exchange of results, experiences and developments, and members from countries that are now starting to perform meiobenthic research are increasingly participating in these conferences The website provides information

on upcoming events, new results and the e-mail addresses of all of the members Scientists from remote places that are often cut off from the mainstream of meio-faunal research can also use such electronic media to easily contact their colleagues and access recent literature The development of electronic species registers, iden-

tification guides, and expert lists (e.g., the European Register of Marine Species, ERMS; NEMYS) has enabled easier access in order to solve the diversity problem

of meiofauna Thus, due to the increasing “globalization” of meiofaunal research through new technical achievements, meiofaunal research will be better dispersed into areas hampered by their social or geographical isolation

More detailed reading: Remane (1933); Pennak (1940); Swedmark (1964); Delamare Deboutteville (1960); Ax (1966); Schwoerbel (1967); McIntyre (1969); Coull and Chandler (1992); Gibert et al (eds 1994); Robertson et al (2000c); Rundle et al (2002)

Meiofaunal research, especially meiobenthic ecology, as initiated by Remane,

is a fairly young fi eld Aside from singular and scattered early descriptions

of strange tiny organisms, the fi eld of marine meiofaunal research originated

in the fi rst decades of the twentieth century in Europe, starting with nomic and basic ecological work More complex ecological approaches were characteristic of research carried out between 1960 and 1980 in Europe and particularly in the US Freshwater studies began independently in eastern Eu-ropean rivers, Swiss streams, and North American lakes Marine and freshwa-ter studies of meio benthos developed along different lines and only recently prompted the ecological parallels a common nomenclature Reasons for the relatively late start of multidirectional meiofaunal research may include the inconspicuous nature of meiobenthic organisms and their unspectacular habi-tats This may have confounded the real phylogenetic and ecological roles of meiofauna Today, the International Meiofauna Association and its triennial conferences bring together work in all fi elds of meiofauna research and most scientists that are studying meio benthos

taxo-The Biotope: Factors and Study Methods

2.1 Abiotic Factors (Sediment Physiography)

2.1.1 Sediment Pores and Particles

When describing the habitats of meiofauna, grain size is a key factor since it directly determines spatial and structural conditions and indirectly determines the physical and chemical milieu of the sediment Poorly sorted sediment parti-cles (e.g., sand mixed with gravel and silt) become tightly packed and the inter-stitial pore volume is often reduced to only 20% of the total volume Well-sorted (coarse) sediments contain up to 45% pore volume According to Ruttner-Kolisko (1962), most field samples of unsorted freshwater sand have 40% pore volume

Aside from pore volume, the external surface area of the sediment particles is an important determinant of meiobenthic life It directly defines the area available for the establishment of biofilms (mucus secretions of bacteria, fungi, diatoms, fauna), which, under natural conditions, form the matrix into which the sediment particles are embedded Thus, particle surface is an important parameter for microscopic animal life This internal surface is unbelievably large: for a 1-m3 stream gravel it has been calculated to amount to about 400 m2 One gram of dry fine sand with a median particle diameter of 63–300 µm may have a total surface area of 8–12.5 m2;

if it consists mostly of diatom shells, this value can even exceed 20 m2, whereas for

1 g of coarse-grained calcareous sand a value of just 1.8 m2 was calculated (Suess 1973; Mayer and Rossi 1982)

In addition to size, the grain shape also determines the sorting of the sediment Angular, splintery particles are packed tighter than spherical ones A higher angu-larity leads to more structural complexity, less water permeability and usually higher abundance of meiofauna (Fig 2.1; see Conrad 1976) A direct correlation between pore dimensions and body size of meiofaunal animals has been demon-strated experimentally (Williams 1972) In general, mesobenthic species moving between the sand grains prefer coarse sands, while endo- and epibenthic ones are

© Springer-Verlag Berlin Heidelberg 2009

mostly encountered in fine to silty sediments These sediment differences affect the two major groups of meio benthos, nematodes and harpacticoids The finer sedi-ments are preferred by most nematodes, while coarser ones are often favored by harpacticoids (Coull 1985) Within the nematode taxon, the preference for a spe-cific grain size was found to relate to certain ecological types (Wieser 1959a)

“Sliders” live in the wide voids of coarse sand; below a critical median grain size

of about 200 µm, the interstices become too narrow Thus, fine sand and mud will

be populated by “burrowers” (Fig 2.2) The particle shape determines the tion of the sediment by meiofauna through indirect action via water content and by permeability (Sect 2.1.3)

coloniza-The colonization of sand by meio benthos is also determined by the grain ture, the roughness of edges, and the shapes of grain surfaces and cracks These are important parameters that structure the microhabitats of different bacterial colonies (Meadows and Anderson 1966) Sand grains with diameters of >300 µm frequently have more plain surfaces than smaller particles; they also have a different bacterial epigrowth This diversification has been shown to attract different meiofauna (Marcotte 1986a, Watling 1988) Likewise, in comparative experiments, cores of different grain sizes have been colonized by different meio benthos This empha-sizes the capacity of meiofaunal species to chose and “recognize” their preferred sediment (Boaden 1962; Gray 1965; Hadl et al 1970; Vanreusel 1991) Although the direct structural impact of the sediment particles is mostly confounded by other factors, e.g., biofilms, water flow, etc (see Table 2 in Snelgrove and Butman 1994), there are strong affinities of specific meiofauna for specific sediments (Schratzberger

struc-et al 2004) The structure and dimensions of the pore system are also directly related with the anatomy of the inhabitants and the functions of their organs (Ax 1966; Lombardi and Ruppert 1982)

cor-Fig 2.1 The pore system in sediments consisting of grains with a round shape (glass beads; left)

vs natural grains of angular shape (right); note differences in pore space due to different packing

(After Conrad 1976; modified)

2.1.2 Granulometric Characteristics

2.1.2.1 Grain Size Composition

Grain size analysis is fundamental to all ecological aspects of meiobenthic work Although the fractionation of the sediment into different size groups does not reflect the natural composition, it provides a basis for reference and an important comparative framework Techniques of sediment analysis are well covered in Bale and Kenny (2005); only some additional practical hints are presented here Granulometry is usually based on the rather tedious procedure of the fractionated sieving of a sufficiently large sample Recently sieving has been replaced by electronic procedures (modified Coulter counters, laser diffraction counters) with higher accu-racy and throughput Inherent inaccuracies with sieving (underrepresentation in the finer fractions) are based on effects of the adhesion of particles to the mesh fibers (Logan 1993) Salt-containing marine samples are mostly wet sieved, especially when fecal pellets consolidate fine sediment However, the faster technique of dry sieving is often preferred (80 °C, 24 h) and is sufficiently accurate if agglutination

sediment

Fig 2.2 Distribution pattern of meiofaunal

locomotory groups in the intertidal of a

sandy shore Black areas in circles or

squares relate to the number of species

same locomotor type; lines indicate areas

of identical median grain size (After

Wieser 1959)

is avoided and the salt content of the sample is corrected for The inaccuracies involved in these procedures are acceptable for most ecological questions The silt-clay fraction (“mud content”) passing through the 63-µm or 44-µm sieve is an important ecological parameter that determines the biological and mechanical properties of the sediment, but is usually not differentiated any further After siev-ing, its proportion is determined by the loss of weight However, it can be refined

by performing a fractionated analysis of the settling velocity using elaborate soil science methods

The mesh sizes of the sieve set usually follow a geometric series (Wentworthscale) with 1.0 or 0.5 ϕ (phi) intervals, where ϕ =− log

log

x

2 with x = particle size in mm (Wentworth 1922; Krumbein 1939) Commonly for meiofaunal studies a series of sieves are used with mesh sizes (mm) 1.0/0.5/0.25/0.125/0.063/0.044 (= 0/ + 1.0/ + 2.0/ + 3.0/ + 4.0/ + 4.5 ϕ units) Very small meiofauna (e.g., some nematodes) would even pass through the 0.044-mm sieve and can only be quantitatively retained using a 0.031-µm sieve (= + 5.0 ϕ) Some animals with a smaller diameter than the mesh width are always retained lengthwise on the screen despite the wide meshes A correction factor has been calculated to account for this inaccuracy (Tseitlin et al 2001) With the increasing use of electro-optical devices this problem is has reduced in importance Electronic calculations and illustrations of particle size mean that the ϕ notation is losing relevance

The simple process of sieving has some pitfalls that can render the procedure needlessly tedious or misleading:

(a) It is important to weigh the whole sample as soon as possible to ensure the rect determinations of water content and salinity (see below) If this treatment

cor-is not possible shortly after sampling, care must be taken to keep the fresh core

in a tight bag to minimize the outflow of water and evaporation

(b) Massive shaking of water-unsaturated cores during transport (e.g., due to motor vibrations on boats!) should be avoided because this can alter sediment struc-ture and water saturation considerably

(c) If a sediment core contains a few coarse pebbles or shells in otherwise tively homogeneous and fine sediment, these should be removed Since cal-culations of character indices depend solely on weight, one or two massive particles can completely change the granulometric curve without having a relevant impact on the meiofauna I believe that this alteration of conditions

rela-is justified in biological studies, provided that the manipulation rela-is mentioned

in the text

Block histograms or ternary diagrams (triangular coordinates) are the usual ods used to illustrate particle size distribution (Krumbein 1939; Gray 1981; Bale and Kenny 2005) The relevant granulometric parameters can be computer-calcu-lated using specific software (e.g., Gradistat; Blott and Pye 2001) or calculated by simple mathematical methods: the fractions are computed as cumulative percent-ages starting with the coarsest fraction These values are listed for further mathe-matical treatment or plotted as cumulative frequency curves (Fig 2.3) It is apparent

meth-that the use of the ϕ notation (abscissa) has the advantage of giving relatively more detailed information on the important finer particles, and it also produces equidis-tant intervals that are relevant for the assessment of the following important statisti-cal indices.

The grain size composition of a sample is characterized by a few statistical parameters (see Table 2.3 in Bale and Kenny 2005) which can be read directly from the diagram or calculated These include the median (Md) and the first (Q1) and the third (Q3) quartiles The Md value corresponds to the 50% point of the cumulative scale (ϕ 50), Q1 to ϕ 25 and Q3 to ϕ 75 These values indicate the aver-age grain size and the spread (scatter) of the grain size fractions towards both ends The spread distance is defined by the sorting coefficient and conveniently expressed by the

Quartile Deviation QDϕ =ϕ25−ϕ75

A homogeneous sediment with a small QD enclosing only a few phi-intervals between the quartiles is regarded as “well sorted” (Table 2.1) An ideally sorted sediment would consist just of one grain fraction and would thus have

QD = 0

siliceous sand calcareous sand

Fig 2.3 a–b Granulometric analysis of two exposed Atlantic beaches Open squares, Portugal; solid circles, Bermuda a Cumulative frequency curves b The same granulometric data plotted on

probability paper

The frequency curve will only attain a sigmoid shape if the sediment fractions tend to follow a normal distribution However, it will become “skewed,” i.e., it will have an asymmetrical slope when certain fractions are over- or underrepresented The degree of curve symmetry is measured by the

ϕ Quartile Skewness: Sk =ϕ ( Q1+ Q3)ϕ ϕ − ϕ

The above indices are based only on very few ϕ values, and they tend to neglect the

“tails” of the curve More precise computations comprise a wider portion of the fraction, i.e., the mean,

All granulometric indices (e.g., the values for the median or quartiles) can also

be computed mathematically (Hartwig 1973b) from the listed size frequencies by interpolation or by using computer software In biological papers it is more illustra-tive to convert ϕ values into metric units The use of a conversion chart (Page 1955; Fig 3.2 in Buchanan 1971) or computer software is often recommended, although

calculation is just as easy The calculation of ϕ from x [mm]: −log x/log 2; calculation

of x [mm] from ϕ : x[mm] = 2−ϕ

Table 2.1 Sediment sorting classes (Gray 1981)

The occurrence of certain sediment types varies depending on the local geological and physiographical conditions In temperate and boreal regions siliceous sands prevail, while in the warmer regions and on seamounts inhomogeneous biogenic calcareous sediments with more complex surface structures dominate (see Sect 8.2) Black basalt and lava sand can often be found in volcanic areas The deep sea floor

is usually muddy and fluffy (unconsolidated), often consisting of foraminiferan (mostly calcareous) or radiolarian (mostly siliceous) skeletons In shallow seas, offshore bottoms will usually consist of medium sand while nearer to the shore currents attenuate and will allow fine sand and mud to settle In areas where ripple marks indicate strong currents, crests contain coarser sediments than troughs, where fine sand and often flocculent surface layers with a higher content of organic material tend to accumulate The fine sediment in seagrass beds, where currents are

Table 2.2 Characteristic granulometric indices for the sediment samples plotted in Fig 2.3a,b

The size, shape and composition of sediment particles interact via the water

fl ux with the physical and chemical regime of the sediment, the exposure to currents and waves as well as the general geological setting In this network

of abiotic factors that infl uence the habitat of meiobenthos, grain size plays a dominant role and can serve as the integrative key factor that characterizes the habitat of meiobenthos Although we now know that communities and zones are not defi ned only by grain size composition, and that the differentiating fac-tors are instead chemically and biologically controlled, granulometry remains

an important foundation Angular grains are packed tighter than round ones, but splintery, uneven surfaces are better for microbe colonization Sediments with smaller grains offer less interstitial space and are preferred by different meiofaunal species to those in coarser sands In general, the void system of sediments accounts for 20–45% of the total sediment volume Careful granu-lometry should form the basis for every benthic ecological study Modern data processing programs enable the relevant granulometric parameters, such

as median, mean, quartiles, sorting coeffi cient and kurtosis, to be calculated automatically These describe the granulometric basis for the living condi-tions of the biota and allow for abiotic structural comparisons

weak, is enriched with leaf detritus Near the shoreline the sediment structure may vary rapidly due to irregular water agitation, sedimentation and resuspension of shore vegetation and wrack material These various sediment structures all repre-sent different microhabitats for meiobenthic animals (Eckman 1979; Hogue and Miller 1981; Hicks 1989).

2.1.3 The Sediment–Water Regime

2.1.3.1 Exposure, Sediment Agitation, and Erosion

Largely determined by the impacts of waves and currents, the exposure of a habitat

is of eminent importance for the agitation and sorting of sediment particles, the flow of sediment water and fluxes of nutrients Current velocity, sediment agitation and sorting interact in a complex way with the weights and surface structures of the particles and determine particle deposition and packing These factors, in combina-tion, control the “exposure” of a site, but a direct measurement of exposure is too complicated mathematically and instrumentally to be used by most biologists Thomas (1986) and Hummon (1989) estimated the exposures of sandy shores from

a fetch-energy index which was calculated using wave height and shoreline uration, parameters which can be extrapolated from maps and data sheets Eleftheriou and Nicholson (1975), on the basis of granulometry, discriminated exposed beaches from sheltered and semi-exposed ones via a critical median grain size of 230 µm McLachlan (1980, 1989) attempted to create a general rating sys-tem for beaches based on a set of parameters including the height of the incoming waves Muus (1968) and Doty (1971) related exposure to the weight loss of plaster test blocks distributed in/on the sediment The dissolution of calcium sulfate was considered to be proportional to the velocity of the surrounding water currents, thus reflecting the exposure of the habitat Similarly, Craik (1980) tried to derive the relative degree of (massive) exposure from the long-term scouring of cement blocks Valesini et al (2003) based their assessment of exposure on a set of seven quantitative environmental variables (e.g., fetch, steepness of shore, width of beach), which they analyzed using multivariate statistics, and classified several groups of beaches However, in practice and in studies dealing with heterogeneous sites and topics, this computer-based grouping appears rather complex Exposure remains a more or less summative often even subjective factor Hence, bentholo-gists are well advised to include a significant amount of comparative experience when deriving any measurements of the rate of exposure

config-Current velocity is not directly proportional to agitation and erosion Turbulent water currents reduce particle suspension (McNair et al 1997); particles with a diameter of approximately 180 µm are most easily eroded (Sanders 1958) A thresh-old of around 200 µm, earlier defined as a “critical grain size” for the occurrence

of many animals (see Sect 2.1.1), is of prime importance for the water contents of sediments The lower average grain size threshold for the existence of an interstitial

assemblage is often reported to be 150 µm In freshwater sediments, 250 µm has been considered the size limit for the circulation of interstitial water (Rutter–Kolisko 1961).

Neither tightly packed silt nor permanently agitated coarse sand offer favorable conditions for most meiofauna In the rigid hydrographic regime of a North Sea estuary, increasing tidal ranges and current surges reduced nematode diversity in the sediment, while the biomasses of many species increased (Smol et al 1994) Most but not all meiofauna react to strong currents and water surges by attempting

to escape through downward migration (Steyaert et al 2001; Sedlacek and Thistle 2006) Avoidance reactions of meiofauna to increasing currents and wave action, e.g., tidal wave fronts and concomitant vibrations of the sediment, have been docu-mented and studied in experiments (Fig 2.4; McLachlan et al 1977; Meineke and Westheide 1979; Foy and Thistle 1991) Specialized species only will occur deep

in the muds of sheltered flats or in the swash zones of exposed beaches (Menn 2002a, Gheskiere et al 2005) Massive agitation of the sediment by storms appar-ently destroys the less agile meiofaunal groups

The erosion, shear strength and settling velocity of the sediment are not just influenced by abiotic factors Biogenic factors such as the reworking of the sedi-ment by intensive burrowing and pelletization as a result of defecation contribute considerably to the physical and biological properties of the sediments Fecal pel-lets covering the bottom surface, especially in tidal flats, may reduce sediment shear strength and enhance erodibility by water currents, but they also tend to increase settlement velocity (Rhoads et al 1977; Andersen and Pejrup 2002) Protruding tubes and plant culms may cause water turbulences and erosive forces, sometimes with negative impact on meiofauna (Coull and Palmer 1984; Hicks 1989) Agglutination by mucus (produced by bacteria, microphytobenthos and

Fig 2.4 Migration of beach meiofauna in relation to the tidal cycle (McLachlan et al 1977)

animals) as well as compaction in tube walls by small infauna will solidify the texture, increase sediment stability and diminish resuspension (Rhoads et al 1978; Luckenbach 1986; Meadows and Tait, 1989; Decho 1990; Miller et al 1996, Wiltshire 2000) When diatom populations became massively reduced by browsing

so as to lower their mucus production, the shear strength and sediment cohesion decreased There is a complex and dynamic correlation between the “biostabilizers” (mainly diatoms) and the “biodestabilizers” (mainly bivalves and polychaetes), between the “biosuspenders” (deposit feeders) and “bioirrigators” (tubicolous annelids and crustaceans) (Graf and Rosenberg 1997; Widdows et al 2002; Meysman et al 2006b)

2.1.3.2 Permeability, Pore Water Flow, Porosity, and Bioturbation

Permeability Permeability denotes the potential speed of water flowing through the sediment (volume of water flow per time, cm3 × s−1); in freshwater biology perme-ability is appropriately termed the “hydraulic conductivity.” It is calculated using a permeameter (see Fig 5.4 in Giere et al 1988) Directly influenced by the absolute size of the sand grains, it decreases as the proportion of small particles increases, especially those below 200 µm in diameter The configurations of the individual pores and the structure and coherence of the void system all exert considerable influence on the permeability of the sediment, but permeability is not directly related to porosity (see below) Since water flow determines most chemical and physical factors in the sediment via the exchange rates of interstitial and superna-tant water, permeability is responsible for supplying oxygen and dissolved and particulate nutrients, and so it largely controls the life conditions of meiofauna.Nutrient fluxes caused by pore water drainage through the tides easily exceed dif-fusive or bioirrigative fluxes (Billerbek et al 2006) In exposed sandy beaches, the

“tidal pump” creates a “stormy interstitial,” exposing the interstitial animals to high flow velocities In near-surface layers, the wave-induced advective transport of pore water (>40 cm × h−1) exceeded diffusive transport by at least three orders of magni-tude (Precht and Huettel 2003) Each lengthwise beach meter is percolated by several cubic meters of seawater each day The yearly volume of the global shelf filtered (the

“subtidal pump”) by the forces of percolation far exceeds the precipitation volume on land (Riedl and Machan 1972; Riedl et al 1972) Berelson et al (1999) calculated that within two hundred days the entire water column of Port Phillip Bay, Melbourne (Australia) passes through the sediment In a tidal beach, 1 m2 of coarse sand filtered

14 L of water each hour (Rusch and Huettel 2000), a value also confirmed for Mediterranean shores (Precht and Huettel 2004) Even the small-scale topography of sandy bottoms massively influences advective water flux and particle transport On the exposed sides of sediment mounds or ripple marks, surface water and organic particles penetrated about seven times deeper into the sediment than on the sheltered sides (Ziebis et al 1996; Huettel and Rusch 2000) The small-scale topography also directs the water flow, with intrusion occurring mainly in the ripple troughs and release occurring after filtration at the crests (Precht and Huettel 2004)

The pore water velocity was first assessed by inserting heated thermistors into the sediment (Riedl and Machan 1972); microflowmeters based on minute thermis-tors were later used by researchers (LaBarbera and Vogel 1976; Davey et al 1990) The cooling effect of the currents on a heated wire produces a voltage signal on a monitor, which, after calibration, indicates the microflow of water Similarly, changes in the potential of a platinum wire used to measure the oxygen diffusion rate in sediments can be calibrated to record water microflows Malan and McLachlan (1991) measured the pumping effects of waves and emphasized that most authors have underestimated wave-induced sediment water fluxes and their impact on the oxygen distribution Long-term in situ records with oxygen microelectrodes have also indicated strong tide- and wave-dependent water pressure gradients (Weber

et al 2007) Precht and Huettel (2004) visualized the pore water flow in the field

by applying fluorescent dye to the sediment and measuring it with an optical sensor (optode, see Sect 2.1.4)

Porosity The total pore volume of a sediment core, its porosity or void ratio, depends in a complex way on the shape, sorting and mixing of the particles, and not just on the pore size available to the animals Thus, it is not directly predictable from sieving data alone, but it is, of course, of relevance for physicochemical fluxes

in the sediment For mechanical measurements of porosity see Buchanan (1984) or Bale and Kenny (2005) Porosity profiles can also be calculated using electrodes,

by measuring the resistivity of the sediment lattice (Archer et al 1989)

The velocity of the pore water flowing through the interstitial system does not depend solely on the hydrodynamics of the overlying water The fluxes in the chemical milieu of sediments are strongly influenced by the sediment texture (see below) This, in turn, is controlled by bioturbation, sediment reworking, bioirrigation, and mucilage secretion of the benthic fauna (Graf and Rosenberg 1997; Pike et al 2001; Berg et al 2001; Murray et al 2002; Meysman et al 2006a,b), see below

Bioturbation The biological reworking of sediments by endobenthic organisms, termed “bioturbation,” affects all sediments, limnetic and marine, from shallow tidal flats to deep-sea bottoms In modern ecology, bioturbation is considered a major factor in the engineering of all benthic ecosystems (Meysman et al 2006a) and in the creation of three-dimensional sediment structure (Lohrer et al 2004) Because of its numerous biogeochemical implications, bioturbation probably had a massive influence on the archaic evolution of life (Bottjer et al 2000; Dornbos

et al 2005; see Chap 7)

Among macrobenthos, bioturbation is mostly caused by the burrowing and ging of crustaceans and annelids Bioturbative effects can extend to a sediment depth of >20 cm Extrapolations suggest that in tidal flats the upper 10 cm of the sediment will become completely bioturbated once every three years Depending

dig-on the populatidig-on density, bioturbatidig-on can decrease compactidig-on, and can even destabilize the bottom and increase its erodibility (Widdows et al 2000) It provides

a system of tubes and voids and enhances sediment mixing through particle exchange down to greater depths Even sediment particles from a depth of 50 cm

will be transferred to the surface The burrows of the priapulid Halicryptus

spinulosus or the decapod Trypea (Callianassa) create a “secondary surface” of

0.7 m2 per surface m2 in muddy bottoms (Förster and Graf 1992; Powilleit et al 1994) Transport rates of 40–50 g sediment per individual and day have been recorded through the burrow and void system The subsequent increased water penetration accelerates the transport of solutes and gases more than diffusion (Diaz

et al 1994; Berelson et al 1999; Berg et al 2001) Twenty-five percent of the overall oxygen flux is attributed to the irrigational activity of burrowing animals (Booij et al 1994) Bioirrigative water and solute transport into the sediment can exceed normal diffusion by a factor of ten (Aller 1988; Aller and Aller 1992; Kristensen 1988; De Deckere et al 2001)

Thus, benthic fauna markedly increases the flux of particles and modifies the physical processes (Graf and Rosenberg 1997) This has both beneficial and aggravating effects: organic matter and pollutants can be removed from the sur-face and buried into deeper layers where degradation is slow On the other hand, the export of contaminated pore water is enhanced by bioturbators (Green and Chandler et al 1994; Levin et al 1997) By altering the geochemical system with animal tubes, and particularly through the import of oxygenated water by irriga-tional fluxes into anoxic layers, heavy metal precipitates (sulfides) that are buried

at depth will become dissolved and released into the surficial, oxygenated layers (Green and Chandler 1994) Also phosphates and ammonium compounds are released in considerable amounts from the sediment by bioturbation and bioirri-gation The result is (often undesirable) eutrophication with an enhanced produc-tion of microphytobenthos in the overlying water (Monaghan and Giblin 1994) Bioturbative effects have also been shown to cause an undersaturation of calcites

in the surficial layers, leading to increased shell dissolution and mortality (Green

et al 1998)

Just as the sources of bioturbation are very diverse, their effects on meio benthos are also very complex: negative impacts through disturbance and destabilization, positive ones through the oxygen and organic matter supplied (Green and Chandler 1994; Aarnio et al., 1998, Schratzberger and Warwick 1999; Thistle et al 1999; Koller et al 2006) Using radioactive isotopes and fluorescent dye as tracers, Bradshaw et al (2006) found only minor chemical effects of bioturbation in Baltic Sea sediments compared to those of physical processes On a general scale, the chemical impacts of the biogenic mobilization of buried chemical pollutants on meiofauna have not yet been sufficiently evaluated

While macrofaunal burrows affect the sediment, even the dense net of fine burrows of meiofauna can have a considerable influence on sediment struc-ture and fauna colonization (Reichelt 1991, Fenchel 1996; Jensen 1996) Among meio benthos, effective bioturbators are ostracods, nematodes and, particularly at the surface, harpacticoid copepods Cullen (1973) experimentally demonstrated the bioturbative impact of meiofauna He found that their burrowing activities alone eliminated all surface traces of macrofauna within 14 days In average sandy sediment, the burrowing of meiofauna will completely displace the pore water in 1–3 years (Reichelt 1991) Because of meiofaunal bioturbation the trans-port of solutes with the subsequent stimulation of microbial mineralization was

mm-increased up to threefold compared to molecular diffusion (Rysgaard et al 2000) Meiofaunal activity induces considerable microscale oxygen dynamics along the chemoclines of sediments, as documented by online registration with 2D planar optodes (Oguri et al 2006) Distribution patterns of meiofauna, especially their colonization of deeper, anoxic horizons, have been shown to be highly dependent

on the burrow system providing favorable microhabitats (e.g., Thomson and Altenbach 1993)

Modern methods imaging the animal-made void system and bioturbative effects include the use of X-rays or fluorescence tracer techniques (Diaz et al

1994, Powilleit et al 1994) One (cost-intensive) method of analyzing the positions of sediment cores and visualizing their biogenic tubes and burrows is computer-assisted tomography (Rosenberg et al 2007) An indirect and elegant

com-in situ method of demonstratcom-ing mixcom-ing processes due to animal activity on-lcom-ine

is the recording of oxygen changes by (expensive) optical sensors (Wenzhöfer and Glud 2004)

2.1.3.3 Water Content and Water Saturation

The water content (mass of water in relation to the wet mass of a sample) is linked

to grain size and permeability Fine-grained sediments saturated with water have higher water contents than coarse sands Mud cores often contain >50 weight % of water, while medium sand will only hold about 25% Water content is considered

by Flemming and Delafontaine (2000) to be a universal master variable that is vant to any other sediment parameter (attention: inaccuracies may arise from the incorrect use of “content” and “concentration;” content denotes the mass per unit mass, while concentration is the mass per unit volume!)

rele-Water saturation and water flow play a dominant role in structuring nal settlement If the water content fluctuates the pore water is replaced and the meiofauna are supplied with oxygen and nutrients, while in the deeper, perma-nently water-saturated layers the pore water flow is reduced In tidal shores, the occurrence of meiofauna can become restricted because of insufficient water content Moreover, because of their reduced capillary forces water-unsaturated surface layers cause steep gradients of many abiotic factors, such as temperature and salinity (see Sect 2.1.4), often with negative impacts on the meio benthos Particularly in eulittoral shores at ebb tide, the degree of moisture or the desicca-tion stress often correlates with the distribution of meio benthos Lack of water in the surface horizons can force meiofauna into deeper horizons Many eulittoral meiofauna species adapt to the regular tidal alterations of water content and con-comitant salinity fluctuations with preference reactions and migrations (Fig 2.4; see Sect 7.3, 7.4)

meiofau-McLachlan and Turner (1994), based on Delamare-Deboutteville (1960) and Salvat (1964), suggested a generalized stratification pattern of (South African) beaches and their meiofauna in relation to desiccation and water saturation (Fig 2.5)

(a) An upper “dry sand stratum” is characterized by low water saturation and high fluctuations in temperature and salinity Here, the prevalence of semi-terrestrial, specialized oligochaetes, mites and nematodes is contrasted with the scarcity of harpacticoids and turbellarians.

(b) A partly underlying “moist sand stratum” (“zone of retention” in Salvat 1964) has an alternating water supply with fluctuations in temperature and salinity that decrease in the deeper strata Due to the perpetually well-oxygenated con-ditions in this zone, meiofaunal abundance and diversity, particularly those of harpacticoids, increases

(c) In the “water table stratum” around the ground water layer, the sand is always water-saturated In more sheltered beaches, restricted oxygen content and often brackish salinities lead to a reduced meiofaunal diversity and abundance.(d) The “low oxygen stratum,” where oxygen deficiency can extend down to a considerable depth, develops in beaches with a high content of organic matter; this zone can harbor meiofauna adapted to temporary oxygen depletion (see Sect 8.4)

Variations in this four-strata pattern primarily depend on the beach slope and result

in different patterns of wave energy, particle size and nutrient supply: reflective, dissipative and intermediate beaches (Fig 2.6)

The tidal rhythm, local geography, high temperatures and different amounts of organic content will modify the above gradients In flat-profiled and sheltered

“dissipative” shores with medium-to-fine sand, the zonation is less developed

dry sand

brackish and fresh groundwater

swash zone

water-saturated low oxygen

moist sand

infiltration

Fig 2.5 Stratification of a beach profile related to water content (Compiled from various authors)

Conversely, in the exposed shore conditions of an “erosive” shore, the grained high-energy beaches have a “reflective” profile Here, the waves prevent the occurrence of a low-oxygen stratum in the swash zone (“zone of resurgence,” Salvat 1964) This zone is characterized by intensive infiltration and circulation

coarse-of interstitial water, and by a specialized interstitial fauna coarse-of reduced diversity and abundance This physically controlled assemblage contrasts with the rich, often biologically controlled meiofauna of dissipative shores (Menn 2002b; see Sect 9.4) Usually, moderately well-sorted medium sands provide the habitat with the most diverse meiofauna In coarser sand, the species richness can be rel-atively high but population density may be low Muddy sediments are more chemically controlled and often characterized by rich populations of a limited number of species restricted to the surface layer In sublittoral sediments rich in organic matter, meiofaunal communities may be structured by the lack of pore water-flow and the resulting poor oxygen supply In general, the correlation between hydrodynamic patterns, sediment structure and meiofaunal distribution

is strong enough, particularly in littoral areas, to dominate all other factors It often relates directly to the abundance and diversity of meiofauna, particularly nematodes (Vanreusel 1991, Menn 2002b, Gheskiere 2005)

More detailed reading: Hylleberg and Henriksen (1980); Yingst and Rhoads (1980); Gray (1981); Buchanan (1984); Aller (1988); Giere et al (1988a); Kristensen (1988); Watling (1988); McCall and Tevesz (1982); Hall (1994); McLachlan and Turner (1994); Snelgrove and Butman (1994); Graf and Rosenberg (1997); Widdows et al (2000); Pearson (2001); Cadée (2001); Murray

et al (2002); Reise (2002); Bale and Kenny (2005); Meysman et al (2006a)

Fig 2.6 Different beach types and their factor patterns (After McLachlan and Turner 1994)

2.1.4 Physicochemical Characteristics

2.1.4.1 Temperature

Meiofauna are present in polar ice and tropical coral reefs, in the constantly cold sea and in the supralittoral fringe with frequent temperature fluctuations Nevertheless, extremes of temperature can have a structuring impact on meiofauna, particularly

deep-in exposed tidal shores with their steep vertical thermal gradients However, deep-in sublittoral bottoms the influence of temperature on meiofaunal distribution is normally negligible The steepness of the temperature gradient is strongly related

to permeability (see Sect 2.1.3) In water-saturated boreal mud flats of low ability, surface and deeper layers can diverge widely in temperature, particularly at ebb tide While summer temperatures can rise to >40 °C at the surface, those in the

to the sediment can become dissolved, resulting in eutrophicating or luting effects Secretions and tubes compact the bottom A complex web of particle mixing, in- and outfl ows, biosuspension and biocompaction links the sediment and water column Various stratifi cation patterns have been suggested for tidal shores Based mainly on the beach slope, wave energy and tidal regime, dissipative accreting shores can be distinguished from re-

pol-fl ective erosive beaches by grain size, water content, nutrients and oxygen supply As meiofauna avoid strongly agitated sands, intermediate or dissi-pative beaches will be populated by more diverse and richer meiofauna

depths are only 10–15 °C because of a strong vertical dampening In wintertime, even under thick ice cover, the frozen ground at the surface does not extend beyond the uppermost 5 cm (Fig 2.7) This dampening effect with depth, which is particu-larly evident when calculating monthly ranges (Table 2.3), is important for the existence of meiofauna in climatically harsh biotopes where sensitive species often perform vertical migrations if other conditions like oxygen supply are favorable

On the other hand, many meiofaunal animals are highly resistant to frost, either by supercooling or protective dehydration In Lake Taimyr (Siberia) nematodes and oligochaetes have been reported to regularly survive for months frozen in ice at temperatures of −10 °C or less (Timm 1996) The Alaskan ice worm, a black enchytraeid oligochaete, lives permanently in crevices of ice at temperatures of below 0 °C (Goodman and Parrish 1971) The (terrestrial) Antarctic nematode

Fig 2.7a–b A typical temperature distribution in a boreal beach a Summer aspect b Winter

aspect (After Jansson 1966a)

a

b

Panagrolaimus davidi survives temperatures as low as -80˚C and freezing down to

>80 % of its water bodies (Smith et al 2008) Polar sea ice is a permanent habitat for a rich, specialized “sympagic” meiofauna of ecological importance (Gradinger 1999a, Gradinger et al 2005, see Sect 8.1.1)

Temperature can be conveniently and routinely measured with a variety of pointed semiconductor probes connected to electronic (field) instruments Since only the narrow surface of the thin metal probe is temperature-sensitive, in situ measuring is possible even at a considerable penetration depth without much compaction or displacement of the sediment

2.1.4.2 Salinity

As with temperature, meiofaunal organisms exist under all salinity regimes from freshwater to brine seep areas, from brackish shores to deep-sea bottoms Because many species are able to adapt to a wide range of salinities, there is often even a diverse meiofauna in those critical brackish water zones where Remane (1934) described a minimum number of species, mainly for macrofauna Yet, depending much on the frequence of variations, salinity gradients can strongly determine occurrence and species composition of meiofauna (Ingole et al 1998; Richmond

et al 2007) Habitat-adapted ranges of salinity tolerance or preference have been experimentally found in various meiofaunal species (Giere and Pfannkuche 1978; Ingole 1994; Moens and Vincx 2000b); the physiological capacity for salinity regula-tion was elegantly recorded for some littoral nematodes by Forster (1998) using an optical method based on the interference pattern of body fluids Today the interna-tional salinity unit is PSU (Practical Salinity Units) which corresponds to ‰ S In African volcanic lakes high conductivity (often together with extremes of pH, see below) not only structures the occurrence of different meiobenthic assemblages, it locally excludes the existence of meiofauna (Tudorancea and Taylor 2002)

In tidal shores, the steep vertical and horizontal salinity gradients strongly depend,

as with temperature, on the water permeability of the sediment In muds with their water-saturated fine sediments and much reduced vertical water exchange capacity, the surface salinity at ebb tide can rise up to hypersaline conditions due to evaporation

Table 2.3 Monthly temperature ranges in 1964 at various sediment depths in a Scandinavian beach (Jansson 1967)