Lifestyles and Feeding Biology (The Natural History of the Crustacea) [2, Illustrated] 0199797021, 9780199797028

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Lifestyles and Feeding Biology

The Natural History of the Crustacea Series SERIES EDITOR: Martin Thiel Editorial Advisory Board: Geoff Boxshall, Natural History Museum, London, UK Emmett Duffy, Virginia Institute of Marine Sciences, Gloucester, USA Darryl Felder, University of Louisiana, Lafayette, USA Gary Poore, Victoria Museum, Melbourne, Australia Bernard Sainte-Marie, Fisheries and Oceans Canada, Mont-Joli, Canada Gerhard Scholtz, Humboldt University Berlin, Berlin, Germany Fred Schram, Friday Harbor Marine Laboratory, Seattle, USA Les Watling, University of Hawaii, Honolulu, USA Functional Morphology and Diversity (Volume 1) Edited by Les Watling and Martin Thiel Lifestyles and Feeding Biology (Volume 2) Edited by Martin Thiel and Les Watling

Lifestyles and Feeding Biology The Natural History of the Crustacea, Volume 2

EDITED BY MARTIN THIEL AND LES WATLING

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1 Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford New York Auckland  Cape Town  Dar es Salaam  Hong Kong  Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trademark of Oxford University Press in the UK and certain other countries. Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016

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9 8 7 6 5  4 3 2 1 Printed in the United States of America on acid-free paper

PREFACE

In Volume 1 of this series, we asked the authors to examine the diverse array of body morphologies exhibited by crustaceans and to provide insight into the development and function of the various parts of the crustacean body. In this volume, we are taking the functional studies of crustacean morphology one step further by examining the relationship between the diversity of body designs and the life habits of the animals. All animals are functionally constrained to varying extents by their body morphology. These constraints determine where and how a species can live. Burrowers, for example, need to have not only the appendage design required to move sediment particles, but also the appendages required for moving water through the burrow in order to keep the burrow well-oxygenated. Alternatively, the burrower would need to have a respiratory system that allows the animal to live anaerobically, at least for a period of time. Similarly, adaptations for swimming (or perhaps more accurately, for flotation) are critical for plankton dwellers. Such adaptations may comprise of structures that create sufficient drag so that the animal doesn’t sink when it is not propelling itself forward or the ability to alter its metabolism and store lipids so that buoyancy can be maintained. This volume is aimed at providing a broad view of crustacean lifestyles, and, from this vantage point, increasing our understanding of the significance of features of crustacean morphology. Crustaceans are probably the most diverse of all invertebrate groups, whether insects are included or not. As a result, it would seem that crustaceans should make ideal target organisms for studies of evolutionary development, physiology, or evolutionary ecology and not just phylogeny, as has often been the case in the past. The chapters included here summarize the main ecological details of crustacean lifestyles in all habitat types that crustaceans occupy. In that sense, it is also a modern natural history book, and we hope the stories included will be of interest to crustacean biologists who would like to know more about the animals they study, especially if that study occurs primarily in the laboratory.

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ACKNOWLEDGMENTS

First and foremost, we appreciate very much the efforts of all the authors of chapters in this volume for their dedication to the task of summarizing the lifestyles of the crustaceans of interest to them. We especially thank our editorial assistants, Lucas Eastman and Annie Mejaes, without whose help we would not have been able to complete the task, and also Ivan Hinojosa, for his work designing our front cover. The generous contribution from Universidad Católica del Norte continues to be essential for this project—we are grateful for their unconditional support that makes this project possible. We also thank the unnamed colleagues who freely shared their time to provide valuable comments on the chapters in this volume. As usual with a work of this size, the level of effort required to carry it out meant that our families once again had to endure periods of inattention while we put this book together, and for their patience we are very grateful. Finally, we also acknowledge our publisher, Oxford University Press, for its commitment to the project. Editing of this book was generously supported by Universidad Católica del Norte, Chile.

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CONTRIBUTORS

EDITORS Martin Thiel Facultad Ciencias del Mar Universidad Católica del Norte Larrondo 1281 Coquimbo Chile Les Watling Department of Biology University of Hawaii at Manoa 152 Edmondson Hall Honolulu, HI 96822 USA AUTHORS Shane T. Ahyong Australian Museum 6 College Street Sydney, NSW 2010 Australia School of Biological, Earth and Environmental Sciences University of New South Wales Kensington, NSW 2052 Australia

Paula Beatriz Araujo Departamento de Zoologia Universidade Federal do Rio Grande do Sul Avenida Bento Gonçalves 9500, prédio 43435 91501-970 Porto Alegre, RS Brazil R. James A. Atkinson 3 Hill Street Largs Ayrshire KA30 8DX Scotland UK ex University Marine Biological Station Millport Isle of Cumbrae KA28 0EG Scotland UK J. Antonio Baeza 132 Long Hall Department of Biological Sciences Clemson University Clemson, SC 29634 USA Smithsonian Marine Station at Fort Pierce 701 Seaway Drive Fort Pierce, FL 34949 USA

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x Contributors Universidad Católica del Norte Larrondo 1281 Coquimbo Chile Chiara Benvenuto School of Environment and Life Sciences Room 317, Peel Building University of Salford Salford M5 4WT UK Benny K.K. Chan Biodiversity Research Center Academia Sinica 128 Academia Road Sec. 2 Nankang Taipei 115 Taiwan Alan P. Covich Odum School of Ecology University of Georgia Athens, GA 30602 USA Lucas B. Eastman Facultad Ciencias del Mar Universidad Católica del Norte Larrondo 1281 Coquimbo Chile Rubén Escribano Instituto Milenio de Oceanografía Departamento de Oceanografía Universidad de Concepción Casilla 160-C Concepción Chile Sven Hammann Thünen Institute of Sea Fisheries Palmaille 9 22767 Hamburg Germany Jens T. Høeg Department of Biology Marine Biology Section University of Copenhagen

Universitetsparken 4 DK-210 Copenhagen Denmark Veijo Jormalainen Department of Biology University of Turku FI-20014 Turun yliopisto Finland Brenton Knott (deceased), but formerly at: School of Animal Biology The University of Western Australia 35 Stirling Highway Crawley, WA 6009 Australia Kari L. Lavalli Division of Natural Sciences & Mathematics College of General Studies Boston University 871 Commonwealth Avenue Boston, MA 02215 USA Patsy A. McLaughlin (deceased), but formerly at: Shannon Point Marine Center Western Washington University 1900 Shannon Point Road Anacortes, WA 98221 USA Barbara A. Mejaes Facultad Ciencias del Mar Universidad Católica del Norte Larrondo 1281 Coquimbo Chile P. Geoffrey Moore 32 Marine Parade Millport Isle of Cumbrae KA28 0EF Scotland UK ex University Marine Biological Station Millport Isle of Cumbrae KA28 0EG Scotland UK

Contributors Alistair G.B. Poore School of Biological, Earth and Environmental Sciences University of New South Wales Sydney, NSW 2052 Australia Alastair Richardson School of Biological Sciences University of Tasmania Private Bag 55 Hobart, TAS 7001 Australia Hans Ulrik Riisgård Marine Biological Research Centre University of Southern Denmark Hindsholmvej 11 5300 Kerteminde Denmark Ramiro Riquelme-Bugueño Millennium Institute of Oceanography Universidad de Concepción PO Box 160-C Concepción Chile Ehud Spanier The Leon Recanati Institute for Maritime Studies and Department of Maritime Civilizations Leon H. Charney School of Marine Sciences

University of Haifa 199 Aba Khoushy Avenue Mt. Carmel, Haifa 3498838 Israel Richard B. Taylor Leigh Marine Laboratory University of Auckland PO Box 349 Warkworth 0941 New Zealand Stephen C. Weeks Program in Integrated Biosciences Department of Biology The University of Akron Akron, OH 44325 USA George D.F. Wilson 198 South Maple Street Saugatuck, MI 49453 USA Martin Zimmer Leibniz Center for Tropical Marine Ecology Fahrenheitstr. 6 D-28359 Bremen Germany

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CONTENTS



1. The Role of Natural History in Understanding the Diversity of Lifestyles in Crustaceans  •  1 Les Watling and Martin Thiel



2. Diversity of Lifestyles, Sexual Systems, and Larval Development Patterns in Sessile Crustaceans  •  14 Benny K.K. Chan and Jens T. Høeg



3. The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding  •  35 P. Geoffrey Moore and Lucas B. Eastman



4. Burrow Dwelling in Crustacea  •  78 R. James A. Atkinson and Lucas B. Eastman



5. Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone  •  118 Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel



6. Crustaceans in Mobile Homes  •  145 Patsy A. McLaughlin



7. Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles  •  163 J. Antonio Baeza



8. Predator Adaptations of Decapods  •  190 Kari L. Lavalli and Ehud Spanier



9. Small Free-living Crustaceans  •  229 Richard B. Taylor

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xiv Contents

10. Planktonic Crustaceans: Lifestyles in the Water Column  •  262 Rubén Escribano and Ramiro Riquelme-Bugueño



11. Lifestyles of the Species-rich and Fabulous: The Deep-sea Crustaceans  •  279 George D.F. Wilson and Shane T. Ahyong



12. Lifestyles of Terrestrial Crustaceans  •  299 Alastair Richardson and Paula Beatriz Araujo



13. Freshwater Crustaceans: Adaptations to Complex Inland Habitats and Species Interactions  •  337 Alan P. Covich



14. Crustaceans of Extreme Environments  •  379 Chiara Benvenuto, Brenton Knott, and Stephen C. Weeks



15. Filter-feeding Mechanisms in Crustaceans  •  418 Hans Ulrik Riisgård



16. Deposit Feeding: Obtaining Nutrition from Sediment  •  464 Les Watling



17. Lifestyles of Detritus-feeding Crustaceans  •  479 Sven Hammann and Martin Zimmer



18. Grazers of Macroalgae and Higher Plants  •  502 Veijo Jormalainen



19. Foraging Behavior of Crustacean Predators and Scavengers  •  535 Lucas B. Eastman and Martin Thiel Index  •  557

Lifestyles and Feeding Biology

A

B

C

D

E

F

Fig. 3.3. Confocal and scanning electron micrographs illustrating amphipod, tube, and details of amphipod silk fibers. From Kronenberger et  al. (2012a), obtained with permission from Springer. (A)  Confocal micrograph of Crassicorophium bonnellii stained with carmine. Arrows indicate two of four secretory legs (p3 and p4) involved in secreting and spinning amphipod silk; scale bar is 500 μm. (B) Illustration showing C. bonnellii inhabiting its tube, holding a sand grain with its antennae and gnathopods; scale bar is 500 μm. (C) Scanning electron micrograph showing a typical open-ended amphipod tube; scale bar is 500 μm. (D) Scanning electron micrograph showing a net of C. bonnellii silk fibers spun to cement the tube’s sand grains together; scale bar is 50 μm. (E) Scanning electron micrograph illustrating the silk net in more details; scale bar is 10 μm. (F) Scanning electron micrograph showing detail of silk fibers; scale bar is 1 μm.

A

B

D

E

G

H

J

C

F

I

K

L

Fig. 8.4. Crypticity of benthic decapods. (A)  Penaeid shrimp, Heteropenaeus spp. colored to appear as vegetation; hippolytid shrimp (Tozema armatum and Saron spp.) coloration when on (B)  algae or (C)  hard substrate. (D)  Palemonid shrimp (Periclemenes amboinensis) on crinoid. (E)  Periclemenes amboinensis mimicking a crinoid. (F)  Crangon shrimp (Vercoia interrupta) cryptically shaped as snail shell. (G)  Pandalid shrimp (Miropandalus hardingi) with tubercles to mimic shape of host. (H) Pilumnus longicornis with sand entrapped on its hairy carapace. (I) Pugettia producta on seaweed. ( J) Rhinolithodes wosnessenskii and (K) Xantho impressus sculpted to look like rocks. (L) Disruptive coloration demonstrated by cleaner shrimp. A–H, courtesy of Guido T. Poppe and Philippe Poppe: www.poppe-images.com; I, courtesy of John Stachowicz; J and K, photos by authors; L, courtesy of Michael Childress.

A

B

C

D

E

F

Fig. 11.3. Deepwater decapods. (A) Tanner crab (Chionoecetes tanneri); photo courtesy of Monterey Bay Aquarium Research Insitute (MBARI); (B) squat lobster (Munidopsis albatrossae); photo courtesy of MBARI; (C) king crab (Paralomis verrilli); photo courtesy of MBARI; (D) hermit crab (Parapagurus latimanus with zoanthid (Epizoanthus sp.), photo courtesy of S.  Ahyong; (E)  clawed lobster (Acanthacaris tenuimana); photo courtesy of National Oceanic and Atmospheric Administration; and (F) blind lobster (Polycheles amemiyai); photo courtesy of T.Y. Chan.

Fig. 11.5. Benthopelagic isopods. Seafloor (left) and laboratory photographs (right) of two benthopelagic isopods found off the California coast: Munnopsurus (top) and Paropsurus (bottom). Photos courtesy of K. Osborn and MBARI.

A

B

C

D

Fig. 12.1. Examples of terrestrial crustaceans. (A) Landhopper Mysticotalitrus tasmaniae. Photo courtesy of Maria Moore. (B) Oniscidean Benthana cairensis. Photo courtesy of Paula Araujo. (C) Terrestrial crayfish Engaeus orramakunna. Photo courtesy of Niall Doran. (D) Robber crabs Birgus latro. Photo by Alistair Richardson.

Fig. 13.2 Acanthaogammarus maximus, an endemic Lake Baikal amphipod. The spinose morphology is characteristic of this endemic species that grows to 70 mm in length. It is a predator that feeds on small prey within the sediment and is likely protected from some of its predators by its sharp spines.

A

B

1 mm

C

1 mm

D

1 mm 1 mm

Fig. 13.4. Invasive crabs in freshwater habitats. Rhithropanopeus harrisii collected in the Miraflores Third Lock Lake adjacent to the Panama Canal. (A) Male specimen, 17.1 mm carapace width, dorsal view. Photo by of A. Anker. (B)  Ovigerous female specimen, 7.8  mm carapace width, dorsal view and (C)  ventral view. (D)  Juvenile, 2.25 mm carapace width, dorsal view. Photo courtesy of D.G. Roche, from Roche and Torchin (2007). 

A

B

C

D

Fig. 17.1. Examples of detritivorous crustaceans. (A)  Porcellio scaber (Isopoda:  Oniscidea:  Porcellionidae). Courtesy of Sören Franzenburg. (B)  Asellus aquaticus (Isopoda:  Asellota:  Asellidae). Courtesy of Martin Zimmer. (C) Traskorchestia deshayesi (Amphipoda: Gammaridea: Talitridae). Courtesy of Raja Djelassi. (D) Gecarcoidea natalis (Decapoda: Grapsoidea: Grapsidae). Courtesy of Stuart Linton.

A

B

C

Fig. 19.7. Crustacean predatory weapons. (A) Arrow: an example of the stomatopod hammer. From Silke Baron, filed under Creative Commons License. (B) Arrow: an example of the stomatopod spear. Courtesy of Roy Caldwell. (C) Gray fill: the putative injecting apparatus in the remipede Speleonectes tanumekes. From van der Ham and Felgenhauer (2007), with permission from B.E. Felgenhauer.

1 THE ROLE OF NATURAL HISTORY IN UNDERSTANDING THE DIVERSITY OF LIFESTYLES IN CRUSTACEANS

Les Watling and Martin Thiel

Abstract Natural history studies of crustaceans were very popular in the late 1800s and early 1900s, with several books written to educate the general populace about the life habits of ordinary and extraordinary members of the group. These books led to faunal guidebooks, but the latter eventually only covered morphological features that could be used to identify animals captured in the field. Almost all habitats are occupied by crustaceans of one kind or another, and so crustaceans are easily obtainable for study. Natural history studies of crustaceans in their natural habitat are important for setting boundaries on theories of behavior and evolution, but these kinds of studies, although needed, are often no longer conducted by modern biologists. The chapter highlights a few examples showcasing the value of rigorous natural history studies in promoting crustaceans as model organisms that may help to provide the answers needed to preserve our natural heritage and biodiversity.

INTRODUCTION Natural history, according to various dictionaries (e.g., Random House 2010), is the study of organisms and natural objects. Certain definitions go on to expand the area of study to include “their origins, evolution and relationships to one another” (American Heritage Science Dictionary 2002). Even though nowadays natural history studies are not as popular as experimental and reductionist science, in the 1800s these studies were very well-respected, conducted by vocational “biologists” and the general populace alike (Barber 1980). In fact, in Britain it was claimed that those who studied natural history would “become more cheerful, more alert, more interesting. Their temper would be improved by conversing with Nature; their health would be improved by going out into the fresh air” (Barber 1980, p. 17). 1

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Natural History in Understanding the Diversity of Lifestyles in Crustaceans Obtaining the knowledge necessary to understand the natural world required books and papers written by specialists. For crustaceans, the problem was twofold. Apart from crabs and lobsters, many crustaceans are moderately small, and, although daphnias could be found in ponds and observed during an “evening at the microscope” (Barber 1980), only those marine crustaceans that could be found in tide pools were likely to become reasonably well known. As a consequence, certain encyclopedic treatments of the group became very popular. One of the earliest of these comprehensive treatments of crustaceans was the Histoire Naturelle des Crustacés by M. Milne-Edwards (1834). Most of the text is devoted to explaining the anatomy of the diverse crustacean groups (an aspect of crustacean natural history studies that seems to be required even today), with behavioral observations included where the information was known, as exemplified by this short description of decorator crabs: “Les Inachus sont des Crustacés de petite taille qui habitant nos côtes et se tiennent ordinairement dans des eaux assez profondes; on en trouve souvent sur les bancs d’huîtres situés dans des lieux abrités. Ils ont tout le corps couvert de duvet et de poils auxquels s’attachent sou vent des éponges et des corallines; leur couleur est brunâtre” (The Inachus are small crustaceans that live on our coasts and usually occur in rather deep water; they are often found on oyster beds located in sheltered places. Their whole body is covered with fluff and hairs to which sponges and coralline algae often attach; their color is brownish; p. 287). One of the earliest books summarizing lifestyles and behaviors of crustaceans is the volume T.R.R. Stebbing (1893) wrote for the International Scientific Series. This series spanned a wide range of topics, from geology and physics to biology, and even included a volume on crayfish by T.H. Huxley and another dealing with the nervous systems of jellyfish, starfish, and sea urchins by G.J. Romanes. These books were written for an educated public and contained a wealth of information, much of it likely new to its intended audience. Stebbing’s volume summarizes taxonomic information and the lifestyles of all the malacostracous crustaceans, with the exception of amphipods. When the chapter on Amphipoda was to be written, the volume was already 436 pages. Stebbing was an expert on amphipods, and it appears that he could not in any way curtail what he knew to a mere “chapter,” as he had for the isopods, for example, so he begged off, suggesting that a whole volume should be dedicated to amphipods. That volume never appeared. Reading Stebbing’s volume is to get a rather full classical education in addition to a complete compendium of biological facts. He almost always provides the Greek or Latin derivation of the scientific names, and he sometimes muses on whether the name is entirely appropriate. For example, “The name Oodeopus perhaps alludes to the circumstance that in some of the specimens the feet were beginning to swell or bud out, but for swollen feet the Greeks had already provided the name Oedipus, and Dana had already used this name for another genus of prawns, and other naturalists had used it for other purposes before Dana. The alternative derivation of Oodeopus, as meaning ‘with feet on the ground,’ seems to make the name entirely pointless” (p. 253). Other delights in Stebbing come from the small index phrases at the top of the right-hand pages, which give clues to what might be found on that page and can lead the browsing reader to interesting details or behavioral observations. In the introduction to the chapter on isopods, the page heading is “keeping dark.” What follows is a truly delicious example of the writing of the day:  In proportion to their importance in the economy of the world the Isopoda have hitherto attracted little popular notice. They enjoy still less of popular favour. They are all of retiring habits, never needlessly courting attention, but in general clinging as closely as possible to whatever shelter or holdfast they have adopted. Amidst enormous disparities of size and strength and shape and temper, this prudent love of obscurity, the one feature of the moral character which all of them possess in common is strong evidence that all of them must have sprung from a common origin. They have never tempted mankind to search for them as



Les Watling and Martin Thiel food. . . . Several of the species treat their fellow-inhabitants of the sea with little ceremony, and make up for smallness of size by ferocity of behaviour. It is only to be hoped, as it might be considered certain, that their living victims are immeasurably less sensitive to pain than ourselves. (p. 315)

Stebbing also was creative in imagining shapes and faces in the external patterns of many of his favorite crustaceans, certainly helping the reader in memorizing facts and recognizing species (Fig. 1.1). William T. Calman, Scottish zoologist and keeper of zoology at the Natural History Museum in London, produced a popular book on crustaceans, The Life of Crustacea (1911), which, in addition to being an introduction to the anatomy of each of the groups, detailed many of the behavioral attributes of crustaceans. Calman treats the crustacean groups by habitat type, from the seashore to the deep sea and from freshwater to land. Although informative for the amateur zoologist, his book is more direct with the facts than Stebbing’s and offers little additional commentary. Natural history studies, though, declined steadily throughout the 20th century, especially as ecology developed into an experimental and quantitative science beginning in the 1940s and 1950s (Hagen 1992). A few sources of natural history information could still be found, but these were dwindling in numbers. For example, guidebooks of seashore life were plentiful and still are. Many have been written over the past century, but most spend the great bulk of their pages dealing with anatomy in order to facilitate identification. Very little space is devoted to life habits, not even

Fig. 1.1. “Corystes cassivelaunus (Pennant), a female specimen, with the feature on the carapace slightly accentuated [Herbst]” from Stebbing (1893).

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Natural History in Understanding the Diversity of Lifestyles in Crustaceans identifying what the animal eats or how it moves. An early exception was Arnold’s (1901) Sea-Beach at Ebb-Tide, a wonderful compendium of both sufficient anatomical detail to allow identification and behavioral observations to promote a sense of wonder. For example, here is her description of burrowing by the fiddler crab, Uca minax:  One species, U. minax, constructs an archway over the mouth of its burrow, in which it sits and surveys the surroundings, but quickly retreats when danger approaches. The crab makes its burrow by scraping up the mud or sand and forming it into pellets, which it carries under the three anterior walking-feet on the underside, using the legs on the side moving forward, and the fourth one on the other side, to climb out of the hole. After peering cautiously about, the crab emerges, and carries its load four or five feet away before dropping it; then again looks about before quickly running back; and finally, turning its stalked eyes, looks in all directions and suddenly disappears, soon to appear with another load. (p. 284) Morton and Miller (1968), in their seashore guide The New Zealand Sea Shore, are concerned that too much time is taken up with taxonomy: “We must turn from the taxonomy of these amphipods and isopods to their ecology” (p. 214). The tradition of guidebooks serving as natural history guides most likely reached its pinnacle in Between Pacific Tides by Ricketts and Calvin, first published in 1939, but extensively augmented in the revised edition of 1948. Subsequent editions have been produced over the ensuing years, and the book is widely used in marine biology classes taught all along the west coast of the United States. Much of what has kept this book on the reading lists of students over the decades are the many little stories included about the animals of the shore. For example, when discussing hermit crabs:  The pleasant and absurd hermit crabs are the clowns of the tide pools. They rush about on the floors and sides of the rock pools, withdrawing instantly into their borrowed or stolen shells at the least sign of danger, and so dropping to the bottom. . . . It is a moot question whether or not hermit crabs have the grace to wait until a snail is overcome by some fatal calamity before making off with its shell. Many observers suppose that the house-hunting hermit may be the very calamity responsible for the snail’s demise, in which case the hermit would obtain a meal and a home by one master stroke. (p. 23) Although crustaceans are not featured extensively, similar natural history stories producing insights about their lifestyles can be found in Idyll’s 1964 book, Abyss. (“The reputation is well deserved, since many crabs are pugnacious. The velvet ‘fiddler’ crab Portunus puber, a large swimming crab of the coast of France, has so low a boiling point that the French fishermen call it le crabe enragé,” p. 114.) Nowadays, such well-written books are not often found, and there are few that offer much in the way of natural history observations or, in terms of the current volume, on the lifestyles of crustaceans. But interesting information can be found in specialized sources such as books summarizing the biology of parasites. Many crustacean groups have taken up the parasitic lifestyle, and a good number are either quite unusual (e.g., parasitic castrators) or of commercial importance (copepods on farmed salmon). Thus, there has been a push to understand the biology of parasitic crustaceans, and that information has been detailed in several old and new books (Caullery 1952, Dogiel 1966, Rohde 2005). Another interesting source of behavioral information is the book by Hansell (2005), Animal Architecture, in which materials used and structures created by animals are described. For crustaceans, that includes the burrows of decapods and also the mud whips of the amphipod, Dyopedos monacanthus.



Les Watling and Martin Thiel

DIVERSITY OF HABITATS OCCUPIED There are many fascinating aspects to studying crustaceans, but certainly one that is of importance to biologists everywhere is that crustaceans can be found in a very wide diversity of habitats (Table 1.1). We tend to think of crustaceans as marine or freshwater organisms, aquatic in some way (Chapters 2–11 and 13 in this volume), but there are groups of crustaceans that have managed to occupy virtually all habitats on the landward side of the high tide line as well. Given their ubiquity and easy access, crustaceans from freshwater habitats have become preferred study organisms for early workers. For example, the isopod Asellus aquaticus, common in a variety of freshwater habitats in Northwestern Europe, has been extensively studied by crustacean biologists for more than 100 years (Fig. 1.2). This is clearly highlighted by Unwin (1920): “the fact that A. aquaticus was common in all ponds and streams and easily kept in captivity led me to spend not a little time upon its life and structure” (p. 335). To this day, researchers benefit from these thorough natural history studies that continue to be cited in modern publications on the reproductive biology, evolutionary patterns, and susceptibility to environmental pollution of these well-studied organisms (for A. aquaticus, see Bertin and Cezilly 2003, Verovnik et al. 2004, Bundschuh et al. 2012).

Figure 1.2. The freshwater isopod Asellus aquaticus, widespread throughout northwestern Europe. From Calman (1911).

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Table 1.1.  Major habitats of the world and the crustaceans groups that can be found living in them Taxa

Habitats

Subphylum Class Subclass Superorder Order Suborder

Infraorder

Number of Forest Savanna Shrubland Grassland species

Rocky Areas [e.g. inland cliffs, mountain peaks]

Crustacea Remipedia

24

Cephalocarida

12

Branchiopoda

900

Maxillopoda Thecostraca Cirripedia

1,285

Copepoda

12,000

Mystacocarida

13

Ostracoda

13,000

x

Malacostraca Phyllocarida Leptostraca

40

Eumalacostraca Hoplocarida Stomatopoda

350

Syncarida

200

Eucarida Euphausiacea

90

Decapoda Dendrobranchiata

450

Pleocyemata Caridea

3,270

Brachyura

6,560

Anomura

2,450

Astacidea

650

Palinura

170

Thalassinidea

620

x

X

x

x

X

x

x

X

x x

Peracarida Mysida

1,000

Amphipoda

8,000

x

Isopoda

10,000

x

Tanaidacea

1,500

Cumacea

1,300

Spelaeogriphacea

4

Thermobaenacea

34

x—present, x—common, X—dominant in the respective habitats. Species numbers updated from Thiel and Duffy (2007).

x

Desert

Wetlands Caves and Marine (inland) Subterranean Neritic [including Habitats (submergent ponds, (non-aquatic) nearshore, rivers, continental streams, shelf or etc.] oceanic island)

Marine Oceanic

Marine Marine Marine Artificial— Artificial— Deep Intertidal Coastal/ Terrestrial Aquatic Ocean supratidal Floor (benthic and demersal)

Introduced Vegetation

x x x

x

x

x

x

x

x

x

x

x

x

x

x

X

X

x

x

x

x

X

X

X

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Natural History in Understanding the Diversity of Lifestyles in Crustaceans Although most crustaceans live in aquatic habitats, a few groups have been very successful at invading the margins of those habitats or leaving the aquatic habitat behind altogether. Some species (many amphipods and decapod crabs) are permanent inhabitants of temperate and tropical forests, and land isopods have colonized some desert habitats (see Chapter 12 in this volume). Many species have radiated within freshwaters, and new species are frequently discovered in isolated watersheds (e.g., Phiri and Daniels 2014). The high degree of endemism and growing human impacts on inland waters increasingly threaten many of the freshwater and terrestrial decapod species (Beenaerts et al. 2010). In particular, many of the species from tropical forests and freshwater are highly endangered due to extensive habitat destruction and pollution (Cumberlidge et al. 2009). A few species of crustaceans are with us today because they found refuge in unusual habitats as a result of the rise of bony fishes (Wägele 1989). Spelaeogriphaceans are found in caves with freshwater pools or streams in South Africa, Brazil, and Australia (Gordon 1957, Pires 1987, Poore and Humphreys 2003). Remipedes inhabit saltwater caves, often isolated from the surface by a lens of freshwater (Carpenter 1999). Thermosbaenaceans and certain amphipods are routinely sampled from wells in the Mediterranean region and the islands of the West Indies (Stock 1993). Mystacocarids are found along the coasts of most of the world’s oceans, living among sand grains on beaches (Lombardi and Ruppert 1982), while stygocarids and most bathynellaceans live among the sand and gravel fed by freshwaters, often deep under rivers or streams (Noodt 1970, Schminke 1981). The larger cousins of the latter groups, the anaspidaceans, are found only in streams or freshwater bogs in Tasmania and southern Australia (Swain and Reid 1983). In general, an impressive diversity of crustacean taxa is found in extreme environments (see Chapter 14 in this volume). The deep sea harbors representatives from many of the major crustacean taxa (see Chapter 11 in this volume). Here, food availability is limited, leading early workers to conclude that “all the animals of the deep sea ultimately depend for their food-supply on the rain of dead bodies of surface animals which, as already mentioned, is constantly falling on the sea-bottom” (Calman 1911, p. 120). While we now know that at least around hydrothermal vents food may be abundant, for most of the vast expanse of the deep-sea floor, high-quality food is in limited supply (see also Chapter 11 in this volume). The very thin and long appendages found in many deep-sea crustaceans (Fig. 1.3) are thought to help in gathering food and to provide support on the oozy muds of the sea floor (Calman 1911). The one habitat not occupied by crustaceans is the atmosphere. Crustaceans have not managed to modify their body plan to allow them to fly or even glide. Of course, if one accepts the modern molecular genetic evidence that insects are merely terrestrial crustaceans (Trautwein et al. 2012), then crustaceans, in one form or another, have colonized all habitats.

THE IMPORTANCE OF NATURAL HISTORY STUDIES: MATCHING MORPHOLOGY TO LIFESTYLE In this volume, the lifestyles of crustaceans are detailed. The natural history stories told should be used as a starting point to understand fundamentals of crustacean biology. That is, crustacean evolution has resulted in a wide diversity of body plans. For some reason, crustaceans are not constrained in ways that we see in other arthropods—or other phyla for that matter. For example, given all the modern excitement about trilobites (e.g., Fortey 2000), what doomed the group to extinction could be what certain paleontologists see as a positive aspect of their morphology, the three-lobed body plan. Although much could be done with that body plan, and much was



Les Watling and Martin Thiel

A

B

Fig. 1.3. Common deep-sea crustaceans. (A)  The lobster Thaumastocheles zaleucus, and (B)  the crab Platymaia wyville-thomsoni. From Calman (1911).

(such as the development of the ability to roll into a ball, presumably to escape predation, and the elaboration of the body margins with large protuberances and spines), the trilobite body plan had one singular limitation: all the appendages behind the head were essentially of the same design. In contrast, crustacean thoracic and abdominal appendages can take a wide variety of forms to allow walking, running fast (if sideways), swimming, crawling among sand grains, and more. The ability to tagmatize the body, that is, divide it into functional parts from anterior to posterior, is most likely what allowed crustaceans to diversify and inhabit all types of environments. One might argue that amphipods are at the pinnacle of tagmosis with a body plan that changes every two or three segments. This functional division in body parts and appendages also allowed the enormous diversity in feeding modes found in crustaceans. There is no known food source that is not exploited by

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Natural History in Understanding the Diversity of Lifestyles in Crustaceans crustaceans. They use their anterior body appendages to overcome and process living animals, cut into dead animals, suck up body liquids from host animals, rasp and grind tough plant materials, capture food particles out of the water column, sieve organic matter out of sediments, and employ many other specific strategies to obtain food (see Chapters 15–19 in this volume). By arranging different tasks (e.g., food capture and processing, body grooming, self-defense, reproduction, movement) among their multiple body appendages, crustaceans have managed to exploit food resources and microhabitats not accessible to other organisms. Crustaceans also can move and survive in extreme habitats where few other species can live. Body extensions may also be important for other functions, such as reproduction. Crustacean appendages have been modified for sperm transfer, egg attachment, and incubation of embryos and juveniles. In some species, the females even host their growing offspring on their body, defending them against enemies and providing them with an optimal feeding environment (Fig. 1.4). The fascinating diversity of structure and function does not stop at the appendages and body extensions but extends to the entire body. Many crustacean species have large spines and other protuberances that may have defensive or other functions. In some cases, the morphological adaptations allow the crustaceans to blend with their habitat, and this is not uncommon in species living in association with other organisms (Fig. 1.5). The disparate body plans and the diversification of body appendages have allowed the fascinating morphological radiation of crustaceans, surpassing that of any other living animal group. What is needed, we believe, is an examination of the various crustacean body plans relative to the physical constraints of the environments in which they live. A start can be made by linking the information in this volume with that of Volume 1 (Watling and Thiel 2013) and then moving on to the remaining volumes in this series. Perhaps we will be able to eventually answer some of the intriguing “why”

Fig. 1.4. Female Arcturus baffini with small juveniles attached to its antennae. From Bate and Westwood (1863).



Les Watling and Martin Thiel

B

A

Fig. 1.5. (A) The spider crab Huenia proteus closely resembles the blades of (B) its seaweed host Halimeda sp.. From Calman (1911).

questions about mouthpart design, size and shape of walking and swimming appendages, and the development and use of the carapace fold, among many, many others. In conclusion, careful and high-quality natural history observations of crustaceans can benefit functional morphological and evolutionary studies. Natural history can set realistic boundaries on the theoretical studies of a group (Greene 1986) because there is no point in theorizing about an activity—for example, feeding on certain food types—if the animals in question never engage in that activity. Well-done natural history studies can be the foundation on which theoretical research can be based. As Greene (1986) notes “all predictive hypotheses inevitably arise inductively, either from logical consideration of observations or from some form of imagination” (p. 101). It is useful here, we think, to end with an extensive observation by Greene on the value of natural history studies: Good natural history is a source of timeless, priceless information for the biological sciences. It inspires theory as well as provides crucial data for answers to comprehensive, synthetic problems in ecology, ethology, evolution, and conservation biology. Despite this fact, natural history costs relatively little compared to the resultant benefits. It is too important to be left only to chance observations, unprepared minds, and ancillary benefits of other studies. (Greene 1986, pp. 104–105).

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ACKNOWLEDGMENTS We are grateful to Annie Mejaes for her help with the figures and table, and to Claire Nouvian for the translation of the quote from Milne-Edwards.

REFERENCES American Heritage Science Dictionary. Houghton Mifflin Company. http://dictionary.reference.com/ browse/natural history. Arnold, A.F. 1901. The sea-beach at ebb-tide: a guide to the study of the seaweeds and lower animal life found between tide-marks. The Century Company, reprinted by Dover Publications, New York. Barber, L. 1980. The heyday of natural history, 1820–1870. Jonathan Cape, London. Bate, C.S., and J.O. Westwood. 1863. A history of the British sessile-eyed Crustacea. John van Voorst, London. Beenaerts, N., R. Pethiyagoda, P.K.L. Ng, D.C.J. Yeo, G.J. Bex, M.M. Bahir, and T. Artois. 2010. Phylogenetic diversity of Sri Lankan freshwater crabs and its implications for conservation. Molecular Ecology 19:183–196. Bertin, A., and F. Cezilly. 2003. Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus. Journal of Evolutionary Biology 16:698–707. Bundschuh, M., A. Appeltauer, A. Dabrunz, A., and R. Schulz. 2012. Combined effect of invertebrate predation and sublethal pesticide exposure on the behavior and survival of Asellus aquaticus (Crustacea; Isopoda). Archives of Environmental Contamination and Toxicology 63:77–85. Calman, W.T. 1911. The life of Crustacea. Methuen and Company, London. Carpenter, J.H. 1999. Behavior and ecology of Speleonectes epilimnius (Remipedia, Speleonectidae) from surface water of an anchialine cave on San Salvador Island, Bahamas. Crustaceana 72:979–991. Caullery, M. 1952. Parasitism and symbiosis. Sidgewick and Jackson, London. Cumberlidge, N., P.K.L. Ng, D.C.J. Yeo, C. Magalhães, M.R. Campos, F. Alvarez, T. Naruse, S.R. Daniels, L.J. Esser, F.Y.K. Attipoe, F.-L.Clotilde-Ba, W. Darwall, A. McIvor, J.E.M. Baillie, B. Collen, and M. Ram. 2009. Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges. Biological Conservation 142:1665–1673. Dogiel, V.A. 1966. General parasitology. Academic Press, New York. Fortey, R. 2000. Trilobite: eyewitness to evolution. Knopf, New York. Gordon, I. 1957. On Spelaeogriphus, a new cavernicolous crustacean from South Africa. Bulletin of the British Museum of Natural History, Zoology 5:31–47. Greene, H.W. 1986. Natural history and evolutionary biology. Pages 99–108 in M.E. Feder and G.V. Lauder, editors. Predator-prey relationships. University of Chicago Press, Chicago. Hagen, J.B. 1992. An entangled bank: the origins of ecosystem ecology. Rutgers University Press, New Brunswick, New Jersey. Hansell, M. 2005. Animal architecture. Oxford University Press, New York. Idyll, C.P. 1964. Abyss, the deep sea and the creatures that live in it. Thomas Y. Crowell Company, New York. Lombardi, J., and E. Ruppert. 1982. Functional morphology of locomotion in Derocheilocaris typica. Zoomorphology 100:1–10. Milne Edwards, M. 1834. Histoire naturelle des crustacés, comprenant l’anatomie, la physiologie et la classification de ces animaux, Paris. Morton, J.E. and M.C. Miller. 1968. The New Zealand seashore. Collins, London. Noodt, W. 1970. Zur Eidonomie der Stygocaridacea, einer Gruppe interstitieller Syncarida (Malacostraca). Crustaceana 19:227–244. Phiri, E.E., and S.R. Daniels. 2014. Disentangling the divergence and cladogenesis in the freshwater crab species (Potamonautidae: Potamonautes perlatus sensu lato) in the Cape Fold Mountains, South Africa, with the description of two novel cryptic lineages. Zoological Journal of the Linnaean Society 170:310–332.



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Pires, A.M.S. 1987. Potiicoara brasiliensis: a new genus and species of Spelaeogriphacea (Crustacea: Peracarida) from Brazil with a phylogenetic analysis of the Peracarida. Journal of Natural History 21:225–238. Poore, G.C.B., and W.F. Humphreys. 2003. Second species of Mangkurtu (Spelaeogriphacea) from north-western Australia. Records of the Western Australian Museum 22:67–74. Random House. 2010. Kernerman Webster’s college dictionary, Random House. Ricketts, E., and J. Calvin. 1948. Between Pacific tides, revised edition. Stanford University Press, Stanford, California. Rohde, K., editor. 2005. Marine parasitology. CSIRO Publishing, Victoria, Australia. Schminke, H.K. 1981. Adaptations of Bathynellacea (Crustacea, Syncarida) to life in the interstitial (“Zoea Theory”). International Revue Gesamten der Hydrobiologie 66:575–637. Stebbing, T.R.R. 1893. A history of Crustacea, recent Malacostraca. International Scientific Series, Vol. 71. Appleton and Co., New York. Stock, J.H. 1993. Some remarkable distribution patterns in stygobiont Amphipoda. Journal of Natural History 27:807–819. Swain, R., and C.I. Reid. 1983. Observations on the life history and ecology of Anaspides tasmaniae. Journal of Crustacean Biology 3:163–172. Thiel, M., and J.E. Duffy. 2007. The behavioral ecology of crustaceans. A primer in taxonomy and functional biology. Pages 3–28 in J.E. Duffy and M. Thiel, editors. Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, New York. Trautwein, M.D., B.M. Wiegmann, R. Beutel, K.M. Kjer, and D.K. Yeates. 2012. Advances in insect phylogeny at the dawn of the postgenomic era. Annual Review of Entomology 57:449–468. Unwin, E.E. 1920. Notes upon the reproduction of Asellus aquaticus. Journal of the Linnaean Society of London, Zoology 34:335–343. Verovnik, R., B. Sket, and P. Trontelj. 2004. Phylogeography of subterranean and surface populations of water lice Asellus aquaticus (Crustacea: Isopoda). Molecular Ecology 13:1519–1532. Wägele, J.W. 1989. On the influence of fishes on the evolution of benthic crustaceans. Journal of Zoological Systematics and Evolutionary Research 27:297–309. Watling, L. and M. Thiel, editors. 2013. The natural history of Crustacea, Vol. 1: Function morphology and diversity. Oxford University Press, New York.

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2 DIVERSITY OF LIFESTYLES, SEXUAL SYSTEMS, AND LARVAL DEVELOPMENT PATTERNS IN SESSILE CRUSTACEANS

Benny K.K. Chan and Jens T. Høeg

Abstract Thoracican barnacles colonize highly diverse habitats and exhibit great variation in morphological forms and lifestyles. Most are suspension feeders, using their cirri to capture zooplankton for food, but feeding also extends to predatory, semiparasitic, and purely parasitic modes. Barnacles also exhibit a vast diversity of sexual systems comprising both pure hermaphroditism, and systems in which dwarf males coexist with either hermaphrodites or females. Most of the intertidal species are simultaneous hermaphrodites, which facilitates successful mating in highly dense populations, while dwarf male systems occur principally in the deep sea and in epibiotic forms. This diversity in sexual systems probably resulted from multiple convergent events as a response to environmental and socially determined situations. The ground pattern of cirripede larval development is composed of six naupliar instars and the terminal cypris larva. However, considerable variation exists in the developmental mode as related to feeding and dispersal. The terminal cyprid stage is much more stereotyped in its role for attachment, but structures related directly to differences in habitat choice, such as the shape of the antennular attachment organ, vary widely. Recent molecular studies show that thoracican barnacles have undergone significant convergent evolution in both morphology and lifestyles as a result of environmentally driven evolution.

INTRODUCTION In the 18th century, Darwin (1852, 1854) chose cirripede barnacles as model organisms for studying evolution and phylogeny due to the extensive variation in morphology and lifestyles found in that taxon of highly specialized, sessile Crustacea. For the very same reason, barnacles are today subject to intense studies in morphology, ecology, and evolution. Cirripedes start their life cycle as free-swimming larvae, but adults are sessile and exhibit a wide variety of lifestyles ranging from 14



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Fig. 2.1. Diversity of life forms in thoracican barnacles. (A)  Paralepas, a stalked barnacle with naked capitulum. (B) Ibla is the sister group to all other thoracicans. It has only four capitular plates, which are phosphatic not calcitic as in other barnacles. Lepas are stalked barnacles with five capitular plates. (C) Lepas lives on floating objects and is composed of five capitular plates. (D) Conchoderma have reduced plate size. (E) Scalpellum and (F)  Euscalpellum are often deep-sea species with 13 or more capitular plates. (G)  Altiverruca are asymmetrically shaped barnacles. (H) Octomeris are sessilian barnacles with eight wall plates. (I) Megabalanus and ( J) Tetraclita are intertidal sessilian species, with six- and four-shell wall plates, respectively.

intertidal suspension feeders (acorn barnacles), over many epibiotic forms to some of the most advanced parasites (Rhizocephala) known in the Metazoa. The habitat diversity of thoracican barnacles is especially high; they live on many types of substrata ranging from the uppermost intertidal to the deep sea. As an adaptation to these diverse environmental conditions, they have also evolved diverse morphological forms (Fig. 2.1), lifestyles, and reproductive strategies. This chapter reviews the variation in lifestyles, sexual systems, and patterns of larval development of thoracican cirripedes in relation to their habitats. We use here the traditional taxonomy given in Martin and Davis (2001), but we emphasize that many taxa now appear not to be monophyletic, including the Scalpellomorpha, the Verrucomorpha, and many families within the Balanomorpha (Pérez-Losada et al. 2008, 2014).

MORPHOLOGICAL DIVERSITY AND LIFESTYLES IN DIFFERENT HABITATS Exposed Rocky Shores The intertidal environment encompasses rocky shores, mangroves, and sandy beaches. The rocky intertidal zone often supports a very high diversity of thoracican barnacles (Fig. 2.2A) that

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Diversity of Lifestyles, Sexual Systems, and Larval Development comprise a multitude of balanomorphan species (acorn barnacles) and a few but very successful pedunculated forms. In tropical and subtropical oceans, acorn barnacles of the families Balanidae, Tetraclitidae, and Chthamalidae are the dominant occupiers of the mid and high shores of such exposed environments (Newman and Ross 1976; see Fig. 2.2A). On such shores, these barnacles form dense belts with distinct vertical zonation patterns. Variation in shape and shell morphology is correlated to habitat and exposure, although many details are still poorly understood in quantitative terms. Shells of intertidal acorn barnacles are volcano-shaped, a form that both optimizes surface contact relative to size and reduces the drag forces of strong waves. Multitubiferous shells are found in species of Tetraclita, which may also represent an adaptation to such high-energy intertidal shores. Species of Tetraclitella living on shaded rocks or on the underside of large boulders can have depressed shells that facilitate living in such confined habitats (Fig. 2.2B). Different from Tetraclita, Tetraclitella exhibit diametric growth of the radii in the shell (Ross 1969a). Such diametric growth can result in more depressed or flattened shells, allowing the species to live in narrow crevices or shaded areas. The function of the elevated radii and hollow shell structures found in some species is still unknown (Ross 1969a; see Fig. 2.2B). In intertidal acorn barnacles, the opercular opening is protected by two pairs of thick opercular plates (terga and scuta). These form a movable operculum that can close and allow the barnacle to retain water in the mantle cavity for extended periods of time. The resulting water-tight compartment is critical in reducing heat and desiccation stress during low tides or under adverse salinity conditions (Chan et al. 2001). This special morphology has undoubtedly played a key role in enabling balanomorphan barnacles to dominate the upper rocky intertidal. Species of pedunculated barnacles on high-energy rocky shores seem to have invaded this habitat convergently several times. They comprise only a handful of species but can be highly dominating in their particular habitat. Capitulum and Pollicipes have strong, armored capitular plates and a scaly stalk (Fig. 2.3A), which provide protection against physical stresses and predation pressure on the shores. On the Atlantic coasts of North Africa and Southern Europe and the Pacific coast of North America, species of Pollicipes can be almost totally dominating on the most highly exposed shores. But despite this almost inaccessible habitat, P. pollicipes is an economically highly important food item in Europe (Molares and Freire 2003). Capitulum mitella is associated with rock crevices, with only the capitular parts exposed while the stalks are well protected. Although both Pollicipes and Capitulum are nested deep within the thoracican evolutionary tree, the Ibla species are located at the very base (Pérez-Losada et al. 2008) and display a very different and presumably plesiomorphic morphology. This comprises a soft hairy stalk and only four primary plates (scuta, terga) that are phosphatic, as opposed to the calcitic ones found in all other thoracicans (Reid et al. 2012; see Figs. 2.1B and 2.3B). Somewhat similar to Capitulum, Ibla always lives deep in very narrow crevices and with only the top part of the tergum extended out to the rock surface. On high-energy rocky shores composed of calcium-based rocks (Fig. 2.3C), the stalked barnacle Lithotrya displays a very special adaptation. They are the only boring thoracicans (Darwin 1852; Fig. 2.3D,E), and their burrows, which they inhabit permanently, can reach up to 10 cm in depth (Fig. 2.3E). Lithotrya has eight plates in its capitulum, but the lateral and rostral plates are much reduced as an adaptation to the burrowing life (Darwin 1852; Fig. 2.3E). The base of the stalk (Fig. 2.3E) serves both to extend the depth of the burrow and as an anchor, enabling the barnacle to contract its peduncle into the burrow (Fig. 2.3E). The peduncular surfaces, especially the areas around the basal disc, are equipped with specialized calcite spicules that enable the barnacle to mechanically scrape the wall and thus drill the burrow into the rocks. Glands close to the disc secrete chemicals assisting in the dissolution of the calcium rocks (Dineen 1988). Rocky intertidal species are suspension feeders on plankton, including diatoms and copepods, and they use their six pairs of biramous thoracopods, called cirri, in this activity. The last three to six pairs of cirri are long and slender, allowing them to act as a net for food capture when

Fig. 2.2. (A) Balanomorph barnacles are very abundant on intertidal shores where they often form distinct barnacle belts. (B) Tetraclitella chinensis (with hollows on shell) and T. karande from Taiwan shores. Tetraclitella barnacles have flattened and depressed shells. (C) Fistulobalanus on tree trunks of mangroves. (D) Setal diversity on cirri of intertidal balanomorph barnacles. Intertidal barnacles exhibit high diversity of setae on the first three pairs of terminal cirri, which are well adapted to handle a great variety of zooplankton Scale bars in cm, except D. in μm.

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Fig. 2.3. Intertidal pedunculated barnacles. (A) The scalpellimorph Capitulum mitella has an armored capitulum and peduncle and is found in crevices on rocky shores. (B) Ibla cumingi; a group of individuals seen after breaking off from their crevice. Ibla have four capitular plates and a soft and hairy peduncle. (C)  Calcitic rocky shores in the Philippines, which host the only burrowing thoracican barnacle, Lithotrya. (D) Burrow opening of Lithotrya species, showing the oval-shaped opening. (E) Cross-section of a Lithotrya burrow, showing the whole individual with attachment disc (AD). Scale bars in cm.



Benny K.K. Chan and Jens T. Høeg

the barnacles are immersed during high tides. The first one to three pairs of cirri are modified as maxillipeds, being shorter and with a higher diversity of setae (Fig. 2.2D). The maxillipeds are responsible for collecting the plankton trapped in the cirral net and then transferring it to the mouth appendages. Setae on the maxillipeds of intertidal barnacles include serrulate, pappose, and multicuspidate types (Chan et al. 2008; Fig. 2.2D), and such high diversity of setae allows these barnacles to collect a greater variety of plankton types in the shallow water. Cirrus III in Megabalanus have long serrulate setae, which are believed to form a basket that prevents food loss during transfer and help collect smaller sized phytoplankton (Anderson 1994, Chan et al. 2008, Walley 2012). The real mouthparts comprise mandibles with palps and biramous maxillules and maxillae. They also sport a variety of setae and spines, with some types present only in the Balanomorpha (Høeg et al. 1994). The function of the mouthparts has only been directly observed by Barnes and Reese (1959) and Hunt and Alexander (1991). The maxillae push food particles into the mouth by moving together or alternately in the median plane. The maxillules scrape food off the maxillae, and both they and the mandibles act in tearing apart and macerating food items. The mandibular palps are morphologically separated from the mandible itself, a condition unique in Crustacea. By transverse movements, they serve to free the mandibular and maxillulary setae of food items that have become stuck. Cirral activities of barnacles living on exposed rocky shores (Megabalanus, Tetraclita, Capitulum, and Pollicipes species) are of the prolonged extended type, probably to maximize the capture of plankton in an environment with high-velocity currents and strong waves (Anderson 1994). When the current speed becomes low, these barnacles can perform a pumping action from the scutum and tergum, and food particles are transported into the mantle for feeding (Anderson 1994, Chan et al. 2008). In acorn barnacles (some) mobility of the body allows it to turn quickly when the cirral net is extended and thus react to rapid back-and-forth rhythms in the wave pattern (Trager et al. 1990, 1994). Sheltered Soft Sediment Shores In sheltered intertidal environments, including mangroves and protected sandy shores, the dominant barnacles are species of Euraphia, Chthamalus and the Balanidae (Fig. 2.2C). These habitats have weaker waves and currents than do the open coasts, and barnacles living there have weaker and thinner shells. The radii and alae of these species are not strongly united and often part of the radii can be seen externally at the junctions of shell plates. Species living on mangroves are often found on the underside of leaves and on shaded trunks, where temperatures are more moderate compared to the upper or outer sides. The cirri and setal types of these sheltered shore barnacles are similar to the exposed rocky coast species, but they differ in their cirral activity. In Amphibalanus, Fistulobalanus, and Balanus, this involves active beating, where the cirri extends and retreats into the shells in high-frequency rhythms. Such cirral activity allows these barnacles to capture food in their sheltered habitats without being assisted by ambient water currents (Trager et al. 1990, Anderson 1994). The length of barnacle cirri can also respond to current speed to optimize feeding efficiency (Marchinko 2003, Chan and Hung 2005). Deep Sea In the deep-sea environment, most thoracican species belong to the stalked Scalpellomorpha (Fig. 2.1E,F) or the asymmetric Verrucumorpha (Fig. 2.1G). The family Scalpellidae alone comprises more than 250 deep-sea inhabiting species. They range extensively in size and are often epibiotic on other deep-sea organisms, including crabs, pycnogonids, sea urchins, and mollusks (Figs. 2.1E,F and 2.5C,E), but reliable biological information exists only for a handful of species. The large-sized Scalpellum stearnsii (Fig. 2.1E) is commonly found at 200–800 m of the northwestern

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Diversity of Lifestyles, Sexual Systems, and Larval Development Pacific region (Pilsbry 1890). In the Atlantic Ocean, Scalpellum scalpellum is somewhat exceptional in occurring mostly in fairly shallow waters, with a range extending down to about 40 m depth (Buhl-Mortensen and Høeg 2006, Southward 2008) and therefore easily available for laboratory observation (Spremberg et al. 2012). Scalpellomorph barnacles are heavily armored with capitular plates and scaly stalk that offer protection against predation. The stalk allows the barnacle considerable freedom to move or swing. Scalpellid species are suspension feeders and believed to mostly capture large-sized deep-sea planktonic organisms. Scalpellum scalpellum can catch both crustacean nauplii and phytoplankton (personal observation). As in all non-balanomorphan barnacles, only the first pair of cirri are modified as maxillipeds in scalpellids, and the remaining five pairs form the cirral net. Cirral setal types in scalpellids are mainly serrulate and simple setae and thus less diverse than their intertidal counterparts (Chan et al. 2008). This is probably due to scarcity and the lack of diverse types of food sources in the deep-sea environment. The deep sea also hosts stalked barnacles of Heteralepas, which have an almost naked capitulum. At deep-sea hydrothermal vents, the basal energy of the food chain is derived from chemosynthetic bacteria. Barnacles endemic to these habitats appear to rely on the chemosynthetic bacteria for food, and at least Leucolepas longa can directly garden them on their cirri (Southward and Jones 2003). From molecular analysis (Pérez-Losada et al. 2008), it is known that all pedunculated and asymmetric barnacles endemic to vent and seep habitats (Ashinkailepas, Leucolepas, Volcanolepas, and Neoverruca) form a monophyletic unit and may therefore have invaded these environments during a single evolutionary event. Within the Balanomorpha, Eochionelasmus represents a separate invasion of vent habitats.

SYMBIOTIC BARNACLES Associations with Corals Coral-associated barnacles represent a major part of acorn barnacle radiation. According to present taxonomy, there are two separate groups associated with scleractinian corals. The archaeobalanid genus Armatobalanus contains several coral-associated species, whereas the large family Pyrgomatidae contains all other species exclusively living in coral skeletons (except Pyrgosella on sponges) (Fig. 2.4A–D). The molecular phylogenetic evidence of Simon-Blecher et  al. (2007) placed Armatobalanus deep within the Pyrgomatidae, and it therefore appears that all barnacles associated with scleractinians belong to one monophyletic unit. Wanella associated with milleporan hydrocorals is the sister group to the Pyrgomatidae. Pyrgomatid coral barnacles have low and depressed shell walls, but the base embedded deep into the coral skeleton is tubular or cup-shaped (Darwin 1854; see Fig. 2.4A–D). The shell plate morphology is diverse, ranging from a four-plated wall (Cantellius, Creusia, Galkinius) to all wall plates fused together (Savignium, Nobia, and Darwiniella). The scuta and terga can be fused or separated, depending on the species (Chan et al. 2014a). The external shell surface of coral barnacles is overgrown by coral tissue, and different species resort to various means to keep their opercular openings free of tissue. Species of Armatobalanus extend and withdraw their long cirri out of the opercular rim, and this, combined with chopping action of the pronounced tergal beaks, serves to mechanically remove the coral tissue at the rim of the opercular aperture. Some species of the Pyrgomatidae, including Cantellius, have an erected apertural frill, which is an elaboration of the tergal scutal flaps that extends out of the shells and contacts the coral tissue at the opercular rim (Fig. 2.4B,D). This frill is believed to have inhibitory action against coral tissue overgrowing the opercular openings (Anderson 1992). In Savignium and

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Fig. 2.4 Coral and sponge associated barnacles. (A) Wanella milleporae is exclusive on fire corals. (B) Nobia grandis in Galaxia coral species. (C) Savignium on the Favia coral species. (D) Cantellius porita coral species. (E) Euacasta, a sponge barnacle, with cirri extended out of the opercular opening. (F)  Whole shell of the sponge barnacle Euacasta dissected from the sponge tissue. (G) An Acasta species, with large windows (wd) on its base. (H) Cirrus IV of Acasta species, showing the serrated segments on the inner ramus.

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Diversity of Lifestyles, Sexual Systems, and Larval Development Wanella, the inner side of the tergum has glandular tissue believed to release chemicals that prevent such overgrowth (Anderson 1992). Pyrgomatid barnacles are mainly suspension feeders, but some also feed on the mucus produced by corals polyps. Coral barnacles and their hosts exhibit symbiotic relationships. Stable isotope ratios of 12C and 13C (Achituv et al. 1997) suggest that corals contribute a carbon source to the barnacles, demonstrating that the barnacles feed on the coral organic matter and zooxanthellae expelled by the corals. On the other hand, ammonium excreted by the coral barnacles was well absorbed by the coral zooxanthellae for growth (Achituv and Mizrahi 1996). As in all species of the Balanoidea, suspension-feeding coral barnacles have their six pairs of cirri organized into three anterior pairs of maxillipeds and three posterior pairs forming the cirral net. Anderson (1980, 1992) studied the cirral activity of different species of coral barnacles. Dipping cirral beats are characteristic for pyrgomatids, but different species perform active vertical or rostrocarinal dipping actions to collect zooplankton. Such variation in the function of the cirri underlines the extensive morphological variation seen within coral barnacles (Anderson 1992). The molecular-based phylogeny of Simon-Blecher et al. (2007) showed that reductions in the number of shell plates and modifications of the opercular valves have been subjected to much homoplasy in coral barnacle evolution. Hoekia is believed to feed exclusively on the coral tissue overgrowing the opercular opening, thus their cirri are no longer used for feeding and have become much reduced (Ross 1969b). Hoekia monticulariae has only one pair of short, biramous cirri that cannot function in suspension feeding, and the remaining five pairs of cirri are rudimentary. The mouthparts are well-developed, with a mandible and maxillule having saw-like blades in their cutting margin. Associations with Sponges Barnacles of the subfamily Acastinae are obligatorily associated with sponges (Kolbasov 1993) and live inside their tissue. The opercular openings are connected to the outside environment via an opening of the sponge tissue, which allows extension of the cirri for feeding (Fig. 2.4E). Sponge barnacles have a cup-shaped base, and the whole body is spherical and totally embedded into the sponge tissue (Fig. 2.4F). The shell plates are nontubiferous and thinner than open intertidal or coral barnacles. Some species even feature large windows on their shell plates, thus the barnacle body is not totally armored (Fig. 2.4G). Such reduction in strength and coverage of the shell plate armor probably reflects their protected residence within the sponge symbiont. Sponge barnacles are suspension feeders with a 3 + 3 division of maxillipeds and a cirral net. Most species have a serrated inner side of the fourth cirri, but the exact function of this special trait is not known (Fig. 2.4H). It may be used for mechanical scraping of sponge tissue on their opercular rim to avoid overgrowth of the opercular opening (Anderson 1992; see Fig. 2.4H). Sponge barnacles often have a large-beaked tergum, and this is also a structure used to prevent overgrowth of the opercular opening by sponge tissue, similar to that seen in the coral-inhabiting Armatobalanus species. When the barnacle dies, the whole body is overgrown by sponge tissue, and such dead barnacles can often be found in deeper parts of the host. Associations with Mobile Marine Organisms Barnacles of the family Coronulidae include epibiotic barnacles on sea turtles, dolphins, and whales. Chelonibia species are regarded as turtle barnacles. Chelonibia testudinaria are epibiotic on various vertebrates and invertebrates (Fig. 2.5A,B). Platylepas species have their base embedded in the turtle skin and are often found on the flippers (Hayashi 2012). Species of Coronula are large and exclusively found on whales. Xenobalanus lives on the skin of dolphins, and their base is modified to attach on the skin. Chelonibia patula is often found on crab surfaces (Fig. 2.5D, note Cheang et al. [2013] concluded

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Fig. 2.5. Epibiotic barnacles. (A) Museum display of a marine turtle carrying Chelonibia barnacles. Photo courtesy of K.H. Chu. (B) Magnified view of Chelonibia testudinaria on the carapace. (C) The deep-sea Smilium species (Scalpellomorpha) are epibiotic of deep-sea echinoderms. (D) Chelonibia patula, a common epibiotic species on crab surfaces. (E)  A  deep-sea crab showing two species of epibiotic barnacles, a sessilian Striatobalanus and the stalked barnacle Scalpellum stearnsii. (F) Octolasmis cor forming dense colony on the surface of a crab branchial gill

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Diversity of Lifestyles, Sexual Systems, and Larval Development C. patula and C. testudinaria are conspecific from molecular analysis). There are also stalked barnacles of the genus Octolasmis that are often epibiotic on crustaceans. The capitulum structure varies among species living in these specialized habitats. Octolasmis warwickii have partially reduced capitular plates and attach on the surface of crabs and lobsters. In contrast, O. angulata and O. cor live on the gills of crabs and have their capitular plates much reduced, probably due to the absence of predators (Fig. 2.5F). Only species from two genera can be said to be parasitic. The monotypic Anelasma parasitize dogfish sharks, where they are embedded in the tissue either at the gill openings or behind the dorsal fin. The peduncle extends into the host where it serves to absorb food in a manner believed to parallel rhizocephalan barnacles (Høeg et al. 2005, Rees et al. 2014). Interestingly, Anelasma retains cirri although evidently in a rather reduced form without many setae, and it also sports an alimentary canal with mouth and anus. This species therefore seems to represent the only intermediate stage of evolution into parasitism found in cirripedes. Rhizolepas, with two species, parasitizes polychaetes and also has a root system inside the host and cirri that are nothing but simple branches without any setae.

SEXUAL SYSTEMS Cirripedes exhibit a striking variety of sexual systems (Høeg et al. 2009). This variation is especially pronounced within thoracican barnacles and is seen as an adaptation to sessile life in highly different habitats (Yusa et  al. 2012). Thoracican sexual systems comprise simultaneous hermaphroditism, androdioecy (males and hermaphrodites), and dioecy (males and females), but where males exist there are always dwarf males permanently attached to a large hermaphroditic or female partner (Kelly and Sanford 2010, Yusa et al. 2012). Self-fertilization seldom occurs in barnacles. Sexual systems have been subject to much change during the evolution of the Thoracica, and one principal factor is believed to have been mating group size (Pérez-Losada et al. 2008, Yusa et al. 2012). Yamaguchi et al. (2008, 2012a,b) and Urano et al. (2009) developed mathematical models to examine factors affecting the evolution of thoracican sexual systems, and this was tested on natural populations by Yusa et al. (2012). When mating group size (MGS) is large (≈ high population density), barnacles tend to have simultaneous hermaphroditic systems. As MGS decreases, evolution favors first the rare condition of androdioecy, where the population comprises both dwarf males and hermaphrodites, and, ultimately, dioecy, where large females carry dwarf males. One reason for this trend is that as MGS decreases toward 1 (i.e., most individuals are solitary), it becomes increasingly unfavorable for hermaphrodites to invest in male function, resulting in the evolution of pure females. Similarly, at low MGS, there is a high fitness for developing into a dwarf male because it reaches sexual maturity fast, is assured of a mating partner, and does not compete with male function in nearby hermaphrodites. Most species inhabiting the intertidal and shallow water environment form very dense populations and exhibit a system of simultaneous hermaphroditism. Examples are species of the Balanidae, Tetraclitidae, and the stalked barnacles Capitulum and Pollicipes. In this sexual system, all individuals simultaneously develop both male sexual organs (penis, seminal vesicles, and testis) and female sexual organs (ovary) throughout their adult life. The sessile lifestyle has also favored the evolution of an extremely long penis to increase the number of partners available for copulation (Fig. 2.6A). An individual barnacle acting as female will allow the penis to enter through its opercular slit and fertilize the eggs in its mantle cavity, and each individual will often have several potential mating partners within reach (Fig. 2.6B,C). Under such conditions, fitness of male function will be limited by the number of eggs available in the surrounding females. Individuals sitting outside mating distance are prevented from reproduction, but under high population density (high MGS) this is a rare condition. In the deep sea, thoracican barnacles often occur at very low population densities, where a large fraction of individuals live alone, that is, outside mating distance with a nearby partner. Under this

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Fig. 2.6. Sexual systems of barnacles. (A)  Male-behaving sessilian barnacle individuals of Amphibalanus amphitrite using long penis to mate with the female-behaving individual within the mating group. Photo courtesy of Jacky Yu. (B)  Octolasmis angulata, living in dense colonies on crab gills, are hermaphrodites without any dwarf males. (C) Mating between two hermaphrodites of Octolasmis cor. (D) Sac-like dwarf male on a female Scalpellum stearnsii (E). (F) Chelonibia testudinaria, epibiotic on turtles, with depressions on external shells housing dwarf males (indicated by black arrows). (G) Chelonibia patula crab surface have dwarf males on its shell surface. (H) Megalasma striatum, living on sea urchin spines; a large hermaphrodite carrying a dwarf male on its scutal edge.

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Diversity of Lifestyles, Sexual Systems, and Larval Development condition, evolution favors a system in which dwarf males are permanently attached to either hermaphrodites or females. Darwin (1852) was the first to describe such dwarf male systems in scalpellid barnacles, and they were recently surveyed in this family by Buhl-Mortensen and Høeg (2006). In the scalpellid subfamily Calanticinae, the males can have plates emulating those of the hermaphrodites and may also carry reduced cirri. But in the Scalpellinae (200+ species), the males are simple sacs with at most minute terga and scuta (Fig. 2.6D,E). Buhl-Mortensen and Høeg (2013) and Chan et al. (2014c) recently found that scalpelline males have a long cuticular penis that obviously assists in depositing sperm into the mantle cavity of its partner. The mostly shallow-water S. scalpellum exhibits the rare condition of androdioecy (Spremberg et al. 2012). Living at intermediate population densities, hermaphrodite S. scalpellum can often copulate with a nearby hermaphrodite. But the significant fraction of hermaphrodites that sit alone depend entirely on the presence of dwarf males for reproduction. In scalpellines, the dwarf males are normally concentrated in two special areas, the receptacles, located on the rims of the scutal plates (Buhl-Mortensen and Høeg 2006, 2013, Spremberg et al. 2012). The number of males varies with species. In Ornatoscalpellum, there are normally only two, whereas S. scalpellum can carry more than 10 males in either receptaculum. Scalpellum stearnsii differs in having males more randomly distributed along the rim of the mantle orifice, with those located most apically contributing least to fertilizing the brood of the female (Ozaki et al. 2008). The factors that determine the number of dwarf males in scalpellids and the precise location and morphology of the male receptacula are clearly an area that needs closer investigation. The mechanism of sex determination has only been investigated experimentally in S. scalpellum, where it seems that both genetic and environmental sex determination is at play (Svane 1986). All cyprids can apparently settle on free substrata and will then develop into hermaphrodites. But only about 50% of the larval population will settle in the receptacles on hermaphrodites, where they invariably develop into dwarf males (Svane 1986, Høeg unpublished data). For dioecic species such as Trianguloscalpellum regium and S. stearnsii the mechanism of sex determination is completely unknown. According to Gomez (1975), the androdioecic acorn barnacle Conopea galeatha has a genetic sex determination system. When exposed in vitro to an insect juvenile hormone mimic, 50% of the cyprids developed into hermaphrodites and 50% into dwarf males. Dwarf males are rare in the Balanomorpha, presumably because most species have fairly high population densities. But dwarf males (e.g., in androdioecy sexual systems) do exist in some epibiotic acorn barnacles. These males are mostly just hermaphrodites arrested in development and possibly with premature development of the male reproductive structures. Chelonibia testudinaria is epibiotic on the carapace of marine turtles (Fig. 2.6F) and has a rather variable density per host individual. In the wall of shell plates, the radii have developed small depressions where cyprids can settle and develop into dwarf males (Zardus and Hadfield 2004). Similarly, Solidobalanus masignotus, which attaches on algae, houses dwarf males in oval pits on the inner side of its rostrum (Henry and McLaughlin 1967). The turtle barnacle C. patula (= C. testudinaria, see Cheang et al. 2013) also has dwarf males attached on its shell surface (Crisp 1983; Fig. 2.6G). Among stalked barnacles, Octolasmis warwicki is often epibiotic on the surface of crabs, and adult hermaphrodites can carry dwarf males, which resemble small hermaphrodites but never grow to develop female organs (Yusa et al. 2010). A similar pattern exists in Megalasma striatum (Fig. 2.6H). Dwarf males are often more frequently present on solitary individuals, suggesting that cypris larvae can chose to settle on a hermaphrodite and become a dwarf male.

LARVAL DEVELOPMENTAL PATTERN Larval development in barnacles comprises free-swimming naupliar and cypris larvae. The nauplii swim by means of paired antennules, antennae, and mandibles and never develop any postmandibular appendages. The naupliar cuticular shield always carries a pair of frontolateral



Benny K.K. Chan and Jens T. Høeg

horns, a highly complex feature unique to cirripedes (Høeg et al. 2009) but of unknown function (Semmler et al. 2008, 2009). Barnacle nauplii larvae can be either planktotrophic or lecithotrophic, but the cyprids are always lecithotrophic (Chan et al. 2014b). Planktotrophic nauplii are comparatively smaller in size, with well-developed labrum and appendages carrying serrulate setae and basal enditic spines (Fig. 2.7A,B). The advantage of planktotrophy is the production of much larger broods of larvae, where the individual larvae can then increase in size by feeding without energy cost to the parent. Lecithotrophic nauplii are large, allowing storage of copious lipid reserves, but they have a rudimentary labrum and appendages with simple setae and lacking basal enditic spines (Fig. 2.7C,D). In the ground pattern, larval development in thoracicans consists of six naupliar stages and a terminal cypris stage. Most of the species have planktonic naupliar stages, which enable dispersal and thus facilitates a wider geographical distribution. As a typical example, the intertidal species of Tetraclita and Chthamalus need 21–30 days to pass through six naupliar and the single cypris stages (Anderson 1994, Chan 2003, Yan and Chan 2004, Chan and Leung 2007). Some barnacles have an abbreviated development, in which only the cyprids are released to the external environment. In some species, such as the intertidal Tetraclitella divisa, the nauplii are retained inside the mantle cavity until they molt into cyprids (Anderson and Anderson 1985, Chan et al. 2014b). In still other species, the eggs hatch as cyprids, so the naupliar phase is bypassed altogether (Buhl-Mortensen and Høeg 2006). Such abbreviated development, in which only cyprids are released to the external environment, is advantageous in species where habitats have a limited distribution because settlement can occur in the parent population immediately upon release. The brooded nauplii of T. divisa have reduced appendages because they never swim. But planktonic barnacle nauplii can also vary considerably in morphology between species, probably related to differences in both feeding mode and duration of the naupliar phase (Fig. 2.7C,D,E). The cyprid is the terminal larval stage in barnacles, and cyprids are responsible for settlement (Fig. 2.7F). They swim by means of six pairs of natatory thoracopods. Anteriorly, they carry a pair of complexly shaped antennules used for both walking over the substratum and in final cementation (Lagersson and Høeg 2002). Larvae of deep-sea barnacles, whose habitats are mostly rare and patchy, display various modes of larval development (Watanabe et al. 2004, Buhl-Mortensen and Høeg 2006, Yorisue et al. 2013). Arcoscalpellum michelottianum, inhabiting sea mounts, and Neoverruca sp., endemic to hydrothermal vents, have large planktonic but lecithotrophic nauplii that enable dispersal over vast distances of inhospitable seafloor in search of their rare habitats. In contrast, the shell-inhabiting Ornatoscalpellum stroemii, which lives on gorgonian corals, hatch as cyprids that can settle immediately upon release, and this results in very dense local populations. In turtle and whale barnacles, such as C.  testudinaria and Coronula diadema, larval development comprises the ground pattern of six planktonic naupliar stages and a cypris stage (Zardus and Hadfield 2004, Nogata and Matsumura 2006). Because the host substratum of these species is very patchy in the open ocean, larval release may occur in these species when their turtle or whale hosts aggregate in dense populations for mating, thus optimizing the substratum for settlement.

SETTLEMENT AND SUBSTRATUM ATTACHMENT The life cycle of barnacles is biphasic, comprising the planktonic larval phase and the sessile juvenile and adult phase. The ability of the cyprid to locate a site for attachment is therefore pivotal for the continued survival of the attached juvenile and adult stages. Prior to final cementation, the cypris searches for the best site by walking over substratum on its antennules while making frequent stops to examine a local area more closely (Lagersson and Høeg 2002). During these wide and close searching phases, it uses the antennular sensory

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Benny K.K. Chan and Jens T. Høeg

setae located on both the third segment and the laterally projecting fourth segment (Bielecki et al. 2009, Maruzzo et al. 2011). The third segment is specialized as an attachment disc, covered with cuticular villi and hosting the exits of the glands used for adhesion (Fig. 2.7F,G,H). The shape of the attachment disc seems to reflect differences in habitat and substratum choice. It is bell-shaped and near radially symmetrical in intertidal species, but shoe-shaped in deep-sea scalpellid barnacles (Fig. 2.7H). Coral-associated species furnish an extreme example in which the attachment disc is spear-shaped and believed to be used for penetration into coral tissue at settlement (Fig. 2.7G). Both the various settlement factors used by the cyprids in selecting an attachment site and the adhesion mechanism during surface exploration and final cementation are still being very intensely studied, not least due to the practical application of preventing fouling of man-made objects in the sea (Aldred and Clare 2008). In rocky intertidal species, the cyprids are able to place themselves in advantageous areas both in terms of physical properties and vertical zonation and also adjacent to conspecifics, which together ensures both survival and reproductive success (Walker 1995, Clare 2000). Using the antennular sensory organs, the cyprids react to a multitude of cues, including algae and biofilms (Roberts et al. 1991) and the physical properties of the rocky substratum (Raimondi 1988). In these exposed habitats, the cyprids also have a special preference for pits or crevices that may protect against wave action, facilitate water flow for feeding, and shade against excessive insolation (Walker 1995). In some species, notably Semibalanus balanoides, the cyprids react very strongly to the presence of conspecifics, including attached individuals and surfaces previously visited by exploring cyprids (Walker 1995). But, interestingly, they also seem to avoid a zone very close to attached individuals because this ensures that they are less liable to be bulldozed away before they themselves reach a sufficient size (Moyse and Hui 1981). In deeper water species, including the many epibiotic forms, the available substrata are much less frequent and mostly patchily distributed. As detailed above, the type of larval development (e.g., short planktonic phase or release cyprids) may in such forms assist settlement success by retaining the larvae in a local area with suitable settlement sites. But some species are also able to react to a settlement site when this is accidentally encountered even when still in the naupliar phase (Yorisue et al. 2013). The deep-sea barnacle Newmaniverruca albatrossiana, exclusive to sea urchin spines, develops a cypris-type antennule already in the last naupliar stage, and this may enable them to attach prematurely and await final molt to the cypris stage (Watanabe et al. 2008). Neoverruca sp., endemic to active hydrothermal vents, has a long larval development period for effective dispersal (Watanabe et al. 2004). But if stage 6 nauplii detect an elevated temperature (e.g., 10oC) indicating a nearby active vent chimney, they will accelerate development into cyprids compared to development at 4oC (Watanabe et al. 2006). Nauplii of Verruca floridana and Paralepas pedunculata have nauplius eyes even though the adults are deep-sea inhabitants. Although normally used for positive phototaxis only, their nauplii are believed to float up into near-surface waters for dispersal, then sink down to near the bottom for settlement (Bingham and Young 1993). After attachment, a complex metamorphosis occurs because the cyprids and juveniles are so different in morphology that they are functionally incompatible. During this phase, the metamorphosing larvae operate under both energy and time constraints, not least in the intertidal where the larvae are susceptible to desiccation during low tide. It is therefore critical that metamorphosis is passed as quickly as possible, but unfortunately there are very few detailed studies of this process. In Amphibalanus amphitrite, Megabalanus rosa, and the stalked barnacle Lepas, the settled cyprid first went through a quiescent period of tissue reorganization during which the body is raised into a vertical position to the substratum (Høeg et al. 2012, Maruzzo et al. 2011; Fig. 2.7I). In Lepas, this is followed by extension of the peduncle. The juvenile must then free itself from the cypris cuticle by an active process before it can extend the cirri for suspension feeding. In acorn barnacles, the juvenile performs intensely pulsating movements that result in shedding of the cypris carapace at

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Diversity of Lifestyles, Sexual Systems, and Larval Development about 8 h after settlement. Lepas sp. sheds the cypris cuticle 2 days after settlement due to contractile movements of the peduncle. In L.  anserifera, the juvenile actively breaks through the cypris carapace and can therefore remain for several days without impeding cirral feeding (Fig. 2.7I). Shell plate formation commences already (1–2 days) under the cyprid carapace in Lepas. In M. rosa, the free juvenile retains for some time its very thin cuticle and flexible shape, and shell plates do not appear until some time after shedding of the cypris cuticles (Høeg et al. 2012).

OTHER SESSILE CRUSTACEANS AND SESSILE INVERTEBRATES Hermit crabs are commonly known as mobile crustaceans that use gastropod shells for protection. However, there are some hermit crabs that are considered “nonconventional hermit crabs” that adopt the fixed tubes produced by tube worms as shelter. For example, Discorsopagurus schmitti obligatorily inhabits the tubes produced by tube worms Sabellaria cemetarium from the North Pacific coast in Japan to Puget Sound in the United States (McLaughlin 1974). The species of Discorsopagurus are dioecious, having separate male and females. The two sexes have similar size distributions (Gherardi and Cassidy 1994). In the natural environment, the empty tubes for Discorsopagurus are limiting, and Discorsopagurus strongly defend their tubes from invaders using visual patterns (Fiorito and Gherardi 1998). The tube-dwelling hermit crabs prefer having loosened tubes and the change of tubes is related to feeding but not growth, as seen in the typical pattern of mobile hermit crabs. In laboratory experiments, Discorsopagurus can choose gastropod shells for shelter (Gherardi and Cassidy 1994). Living in fixed tubes has many disadvantages when compared to the mobile hermit crabs. Having a fixed location creates difficulties in getting more food, and the tubes are fragile and cannot provide strong protection from predation. It is believed that the tube-dwelling hermit crabs were displaced from gastropod shells to worm tubes by strong competition over evolutionary time. Living in such fixed tubes are the “best of a bad situation” for the tube-dwelling hermit crab species (Gherardi 1996). Living such a sessile mode of life, Discorsopagurus have four feeding techniques including antennary beating (filter feeding), body-trap feeding, feeding on wafting particles, and scraping or deposit feeding (Gherardi 1994). Stomach contents of Discorsopagurus contained suspended and settled detritus, zooplankton, and algae (Caine 1980). Discorsopagurus is thus a generalist and an opportunistic feeder (Gherardi 1994).

FUTURE DIRECTIONS In thoracican barnacles, research on the ecology, behavior, and larval ecology of coral- and sponge-associated barnacles is still in the infant stage. Morphology-based taxonomic studies on coral- and sponge-associated barnacles have been established, but such traditional classification systems should be analyzed using modern molecular approaches. The host specificity of spongeand coral-associated barnacles as revealed from molecular studies (to see if there is host-specific speciation) will be a fruitful area of research in the future. Also, larval morphology, especially of cyprid antennules, has still not been investigated extensively. How the cyprids of coral and sponge barnacles settle and metamorphose on the sponge and coral host is still unknown. Video or time-lapse photography of settlement behavior and metamorphosis of coral and sponge barnacle cyprids will be essential to further understand the ecology of these species. At the level of phylogenetic studies of barnacles, the relationships among lifestyle, habitat use (or host specificity for epibiotic species), sexual systems, and location and morphology of their dwarf males will be an important topic to link to the phylogenetic analysis.



Benny K.K. Chan and Jens T. Høeg

CONCLUSIONS Thoracican barnacles exhibit great diversity in morphology, habitat, lifestyle, development, and sexual systems. This renders them excellent models for studies tracing the evolution of complex biological traits, but such analyses depend on robust phylogenies. Recent molecular-based analyses of major barnacle groups (Pérez-Losada et al. 2008, Yusa et al. 2012) demonstrate that biological features such as sexual systems and many morphological traits (presence of peduncle, numbers of shell plates, asymmetric body shape) have been subject to much parallel or convergent evolution. On the other hand, a surprising result was that most deep-sea hydrothermal and seep barnacles form a monophyletic unit, and this is also so for all acorn barnacles associated with scleractinian corals. Thus, continued development of robust cirripede phylogenies combined with penetrating comparative studies on development, reproduction, and adult morphology and function have every chance of providing insight into the evolutionary radiation of this specialized taxon in terms of both patterns and ultimate causative factors.

REFERENCES Achituv, Y., and L. Mizrahi. 1996. Recycling of ammonium within a hydrocoral (Millepora dichotoma) zooxanthellae-cirripede (Savignium milleporum) symbiotic association. Bulletin of Marine Science 58:856–860. Achituv, Y., I. Brickner, and J. Erez. 1997. Stable carbon isotope ratios in Red Sea barnacles (Cirripedia) as an indicator of their food source. Marine Biology 130:243–247. Aldred, N., and A.S. Clare. 2008. The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling 24:351–363. Anderson, D.T. 1980. Cirral activity and feeding in the Verrucomorph barnacles Verruca recta Aurivillius and V. stroemia (O.F. Muller) (Cirripedia). Journal of the Marine Biological Association of the United Kingdom 60:349–366. Anderson, D.T. 1992. Structure, function and phylogeny of coral-inhabiting barnacles (Cirripedia, Balanoidea). Zoological Journal of the Linnaean Society 106:277–339. Anderson, D.T. 1994. Barnacles—structure, function, development and evolution. Chapman & Hall, London. Anderson, D.T., and J.T. Anderson. 1985. Functional morphology of the balanomorph barnacles Tesseropora rosea (Krauss) and Tetraclitella purpurascens (Wood Tetraclitidae). Australian Journal of Marine Freshwater Research 36:87–113. Barnes, H., and E.S. Reese. 1959. Feeding in the pedunculate cirripede Pollicipes polymerus J.B. Sowerby. Journal of Zoology 132:569–584. Bielecki, J., B.K.K. Chan, J.T. Høeg, and A. Sari. 2009. Antennular sensory organs in cyprids of balanomorphan cirripedes: standardizing terminology using Megabalanus rosa. Biofouling 25:203–214. Bingham, B.L., and C.M. Young. 1993. Larval phototaxis in barnacles and snails associated with bathyal sea urchins. Deep Sea Research Part I 40:1–12. Buhl-Mortensen, L., and J.T. Høeg. 2006. Reproduction and larval development in three scalpellid barnacles Scalpellum scalpellum (Linnaeus 1767), Ornatoscalpellum stroemii (M. Sars 1859) and Arcoscalpellum michelottianum (Sequenza 1876), Crustacea: Cirripedia: Thoracica) implications for reproduction and dispersal in the deep sea. Marine Biology 149:829–844. Buhl-Mortensen, L., and J.T. Høeg. 2013. Reproductive strategy of two deep-sea scalpellid barnacles (Crustacea: Cirripedia: Thoracica) associated with decapods and pycnogonids and the first description of a penis in a scalpellid dwarf males. Organisms Diversity and Evolution 13:545–557. Caine, E.A. 1980. Adaptations of a species of hermit crab (Decapoda, Paguridea) inhabiting sessile worm tubes. Crustaceana 38:306–310. Chan, B.K.K., and O.S. Hung. 2005. Cirral length of the acorn barnacle Tetraclita japonica (Cirripedia: Balanomorpha) in Hong Kong: effect of wave exposure and tidal height. Journal of Crustacean Biology 25:329–332. Chan, B.K.K. 2003. Studies on Tetraclita squamosa and Tetraclita japonica (Cirripedia: Thoracica) II: Larval morphology and development. Journal of Crustacean Biology 23:522–547.

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Diversity of Lifestyles, Sexual Systems, and Larval Development Chan, B.K.K., and O.S. Hung. 2005. Cirral length of the acorn barnacle Tetraclita japonica (Cirripedia: Balanomorpha) in Hong Kong: effect of wave exposure and tidal height. Journal of Crustacean Biology 25:329–332. Chan, B.K.K., and P.T.Y. Leung. 2007. Antennular morphology of the cypris larvae of mangrove barnacle Fitsulobalanus albicostatus (Cirripedia: Thoracica: Balanomorpha). Journal of the Marine Biological Association of the U.K. 87:913–915. Chan, B.K.K., D. Morritt, and G.A. Williams. 2001. Effect of salinity and recruitment on the distribution of Tetraclita squamosa and Tetraclita japonica (Cirripedia: Balanomorpha) in Hong Kong. Marine Biology 138:999–1009. Chan, B.K.K., M. Akihisa, and P.F. Lee. 2008. Latitudinal gradient in the distribution of the intertidal acorn barnacles of the Tetraclita species complex (Crustacea: Cirripedia) in NW Pacific and SE Asian waters. Marine Ecology Progress Series 362:201–210. Chan, B.K.K., R.E. Prabowo, and K.-S. Lee. 2009. Crustacean Fauna of Taiwan: Barnacles, Cirripedia: Thoracica excluding the Pyrgomatidae and Acastinae. National Ocean University Press. Chan B.K.K., Y.-Y. Chen, and Y. Achituv. 2014a. Crustacean Fauna of Taiwan: Barnacles, Cirripedia: Thoracica: Pyrgomatidae. Biodiversity Research Center, Academia Sinica, Taiwan. Chan, B.K.K., J.T. Høeg, and R. Kado. 2014b. Thoracica. Pages 116-122 in J.W. Martin, J. Oleson and J.T. Høeg, editors. Atlas of Crustacean Larvae. John Hopkins University Press, Maryland, USA. Chan, B.K.K., L. Corbari, P.A. Rodriguez Moreno, and D.S. Jones. 2014c. Two new deep-sea stalked barnacles, Arcoscalpellum epeeum sp. nov. and Gymnoscalpellum indopacificum sp. nov. from the Coral Sea, with descriptions of the penis in Gymnoscalpellum dwarf males. Zootaxa 3866:261-276. Cheang, C.C., L.M. Tsang, K.H. Chu, I.-J. Cheng, and B.K.K. Chan. 2013. Host-specific phenotypic plasticity of the turtle barnacle Chelonibia testudinaria: a wide spread generalist rather than a specialist. PLoS ONE 8(3):e57592. specialist. PLoS ONE 8 (3): e57592." Clare, A.S. 2000. Nature and perception of barnacle settlement pheromones. Biofouling 15:57–71. Crisp, D.J. 1983. Chelonibia patula (Ranzani), a pointer to the evolution of complemental male. Marine Biology Letters 4:281–294. Darwin, C. 1852. A monograph on the sub-class Cirripedia with figures of all species. The Lepadidae; or pedunculated barnacles. Ray Society, London. Darwin, C. 1854. A monograph on the sub-class Cirripedia with figures of all species. The Balanidae, Verrucidae, etc. Ray Society, London. Dineen Jr., J.F. 1988. Functional morphology of Lithotrya dorsalis (Cirripedia: Thoracica) in relation to its burrowing habit. Marine Biology 98:543–555. Fiorito, G., and F. Gherardi. 1998. Monitoring near-entrance activity of burrow dwelling invertebrates using an image analysis system. Marine and Freshwater Behaviour and Physiology 31:93–104. Gherardi, F. 1994. Multiple feeding techniques in the sessile hermit crab, Discorsopagurus schmitti, inhabiting polychaete tubes. Oecologia 98:139–146. Gherardi, F. 1996. Non-conventional hermit crabs: pros and cons of a sessile tube-dwelling life in Discorsopagurus schmitti (Stevens). Journal of Experimental Marine Biology and Ecology 202:119–136. Gherardi, F., and P.M. Cassidy. 1994. Sabellarian tubes as the housing of the hermit crab Discosopagurus schmitti. Canadian Journal of Zoology 526–531. Gomez, E.D. 1975. Sex determination in Balanus (Conopea) galeatus (L.) (Cirripedia Thoracica). Crustaceana 28:105–107. Hayashi, R. 2012. Atlas of the barnacles on marine vertebrates in Japanese waters including taxonomic review of superfamily Coronuloidea (Cirripedia: Thoracica). Journal of the Marine Biological Association of the United Kingdom 92:107–127. Henry, D.P., and P.A. McLaughlin. 1967. A revision of the subgenus Solidobalanus Hoek (Cirripedia Thoracica) including a description of a new species with complemental males. Crustaceana 12:43–58. Høeg, J.T., E.S. Karnick, and A. Frølander. 1994. Scanning electron microscopy of mouth appendages in six species of barnacles (Crustacea: Cirripedia: Thoracica). Acta Zoologica 75:337–357. Høeg, J.T., H. Glenner, and J. Shields. 2005. Cirripedia thoracica and rhizocephala (barnacles). Pages 154–165 in K. Rohde, editor. Marine parasites. CABI Publishing, Wallingford U.K. and CSIRO Publishing, Collingwood, Victoria, Australia. Høeg, J.T., M. Perez-Losada, H. Glenner, G.A. Kolbasov, and K.A. Crandall. 2009. Evolution of morphology, ontogeny and life cycles within the Crustacea Thecostraca. Arthropod Systematics & Phylogeny 67:199–217.



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Høeg, J.T., D. Maruzzo, K. Okano, H. Glenner, and B.K.K. Chan. 2012. Metamorphosis in balanomorphan, pedunculated, and parasitic barnacles: a video-based analysis. Integrative and Comparative Biology 52:337–347. Hunt, M.J., and C.G. Alexander. 1991. Feeding mechanisms in the barnacle Tetraclita squamosa (Burguiere). Journal of Experimental Marine Ecology and Biology 154:1–28. Kelly, M.W., and E. Sanford. 2010. The evolution of mating systems in barnacles. Journal of the Experimental Marine Biology and Ecology 392:37–45. Kolbasov, G.A. 1993. Revision of the genus Acasta Leach (Cirripedia: Balanoidea). Zoological Journal of the Linnaean Society 109:395–427. Lagersson, N.C., and J.T. Høeg. 2002. Settlement behaviour and antennulary biomechanics in cypris larvae of Balanus amphitrite (Crustacea: Thecostraca: Cirripedia). Marine Biology 141:513–526. Marchinko, K.B. 2003. Dramatic phenotypic plasticity in barnacle legs (Balanus glandula Darwin): magnitude, age dependence, and speed of response. Evolution 57:1281-1290. Martin, J.W., and G.E. Davis. 2001. An updated classification of the recent crustacean. Natural History Museum of Los Angeles County, Science Series 39:1–124. Maruzzo, D., S. Conlan, N. Aldred, A.S. Clare, and J.T. Høeg. 2011. Video observation of surface exploration in cyprids of Balanus amphitrite: the movements of antennular sensory setae. Biofouling 27:225–239. McLaughlin, P.A. 1974. The hermit crabs (Crustacea, Decapoda, Paguridea) of northwestern North America. Zoologische Verhandelingen 130:1–396. Molares J., and J. Freire. 2003. Development and perspectives for community-based management of the goose barnacle (Pollicipes pollicipes) fisheries in Galicia (NW Spain). Fisheries Research 65:485–492. Moyse, J., and E. Hui. 1981. Avoidance by Balanus balanoides cyprids of settlement on conspecific adults. Journal of Marine Biological Association of the United Kingdom 61:449–460. Newman, W.A., and A. Ross. 1976. Revision of the balanomorph barnacles; including a catalog of the species. Memoirs of the San Diego Society of Natural History 9:1–108. Nogata, Y., and K. Matsumura. 2006. Larval development and settlement of a whale barnacle. Biology Letters 2:92–93. Ozaki, Y., Y. Yusa, S. Yamato, and T. Imaoka. 2008. Reproductive ecology of the pedunculate barnacle Scalpellum stearnsii (Cirripedia: Lepadomorpha: Scalpellidae). Journal of the Marine Biological Association of the United Kingdom 88:77-83. Pérez-Losada, M., M. Harp, J.T. Høeg, Y. Achituv, D. Jones, H. Watanabe, and K.A. Crandall. 2008. The tempo and mode of barnacle evolution. Molecular Phylogenetics and Evolution 46:328–346. Perez-Losada, P., J.T. Høeg, N. Simon-Blecher, Y. Achituv, D. Jones, and K.A. Crandall. 2014. Molecular phylogeny, systematics and morphological evolution of the acorn barnacles (Thoracica: Sessilia; Balanomorpha). Molecular Phylogenetics and Evolution 81:147-158. Pilsbry, H.A. 1890. Description of a new Japanese Scalpellum. Proceedings of the Academy of the Natural Sciences, Philadelphia 42:441–443. Raimondi, P.T. 1988. Rock type affect settlement, recruitment, and zonation of the barnacle Chthamalus anisopoma Pilsbry. Journal of Experimental Marine Biology and Ecology 123:253–267. Rees, D.J., C. Noever, J.T. Høeg, A. Ommundsen, and H. Gelnner. 2014. On the origin of a noel parasiticfeeding mode within suspension feeding barnacles. Current Biology 24:429-434. Reid, D.G., M.J. Mason, B.K.K. Chan, and M.J. Duer. 2012. Characterization of the phosphatic mineral of the barnacle Ibla cumingi at atomic level by solid-state nuclear magnetic resonance: comparison with other phosphatic biominerals. Journal of the Royal Society Interface 9:1510–1516. Roberts, D., D. Rittschof, E. Holm, and A.R. Schimdt. 1991. Factors influencing initial larval settlement: temporal, spatial and surface molecular components. Journal of Experimental Marine Biology and Ecology 150:203–211. Ross, A. 1969a. Studies on the Tetraclitidae (Cirripedia, Thoracica). Revision of Tetraclita. Transactions of the San Diego Society of Natural History 15:237–251. Ross, A. 1969b. A coral-eating barnacle. Pacific Science 23:252–256. Semmler, H., A. Wanninger, J.T. Høeg, and G. Scholtz 2008. Immunocytochemical studies on the naupliar nervous system of Balanus improvisus (Crustacea, Cirripedia, Thecostraca). Arthropod Structure & Development 37:383–95.

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Diversity of Lifestyles, Sexual Systems, and Larval Development Semmler, H., J.T. Høeg, G. Scholtz, and A. Wanninger. 2009. Three-dimensional reconstruction of the naupliar musculature and a scanning electron microscopy atlas of nauplius development of Balanus improvisus (Crustacea: Cirripedia: Thoracica). Arthropod Structure & Development 38:135–45. Simon-Blecher, N., D. Huchon, and Y. Achituv. 2007. Phylogeny of coral-inhabiting barnacles (Cirripedia; Thoracica; Pyrgomatidae) based on 12S, 16S and 18S rDNA analysis. Molecular Phylogenetics and Evolution 44:1333–1341. Southward, A.J. 2008. Barnacles. Pages 1–142 in J.H. Crothers and P.J. Hayward, editors. Synopses of the British fauna (new series). Field Studies Council, Shrewsbury, UK. Southward, A.J., and D.S. Jones. 2003. A revision of stalked barnacles (Cirripedia: Thoracica: Scalpellomorpha: Eolepadidae: Neolepadinae) associated with hydrothermalism, including a description of a new genus and species from a volcanic seamount off Papua New Guinea. Senckenbergiana Maritima 32:77–93. Spremberg, U., J.T. Høeg, L. Buhl-Mortensen, and Y. Yusa. 2012. Cypris settlement and dwarf male formation in the barnacle Scalpellum scalpellum: a model for an androdioecious reproductive system. Journal of Experimental Marine Ecology and Biology 422–423:29–47. Svane, I. 1986. Sex determination in Scalpellum scalpellum (Cirripedia: Thoracica: Lepadomorpha), a hermaphroditism goose barnacle with dwarf males. Marine Biology 90:249–253. Trager, G.C., J.-S. Hwang, and J.R. Strickler. 1990. Barnacle suspension feeding in variable flow. Marine Biology 105:117–127. Trager, G.C., A. Achituv, and A. Genin. 1994. Effect of prey escape ability, flow speed, and predator feeding mode on zooplankton capture by barnacles. Marine Biology 120:251–259. Urano, S., S. Yamaguchi, S. Yamato, S. Takahashi, and Y. Yusa. 2009. Evolution of dwarf males and a variety of sexual modes in barnacles: an ESS approach. Evolution and Ecology Research 11:713–729. Walker, G. 1995. Larval settlement: historical and future perspectives. Pages 69–85 in F.R. Schram and J.T. Høeg, editors. New frontiers in barnacle evolution. Crustacean Issues 10. Balkema, Rotterdam, The Netherlands. Walley, J. 2012. Setal morphology in cirripedes: a useful tool in phylogenetic studies? Journal of the Marine Biological Association of the United Kingdom 92:305–325. Watanabe, H., R. Kado, S. Tsuchida, H. Miyake, M. Kyo, and S. Kojima. 2004. Larval development and intermoult period of the hydrothermal vent barnacle Neoverruca sp. Journal of the Marine Biological Association of the U.K. 84:743–745. Watanabe, H., R. Kado, M. Kaida, S. Tsuchida, and S. Kojima. 2006. Dispersal of vent-barnacle (genus Neoverruca) in the Western Pacific. Cahiers de Biologie Marine 47:353–357. Watanabe, H., J.T. Høeg, B.K.K. Chan, R. Kado, S. Kojima, and A. Sari. 2008. First report of attachment organs in a barnacle nauplius larva. Journal of Zoology 274:284–291. Yamaguchi, S., Y. Yusa, S. Yamato, S. Urano, and S. Takahashi. 2008. Mating group size and evolutionarily stable pattern of sexuality in barnacles. Journal of Theoretical Biology 253:61–73. Yamaguchi, S., E.L. Charnov, K. Sawada, and Y. Yusa. 2012a. Sexual systems and life history of barnacles: a theoretical perspective. Integrative and Comparative Biology 52:356–365. Yamaguchi, S., Y. Yusa, K. Sawada, and S. Takahashi. 2012b. Sexual systems and dwarf males in barnacles: integrating life history and sex allocation theories. Journal of Theoretical Biology 320:1–9. Yan, Y., and B.K.K. Chan. 2004. Larval morphology of the newly identified barnacle Chthamalus neglectus (Cirripedia: Thoracica: Chthamalidae) in Hong Kong. Journal of Crustacean Biology 24:519–528. Yorisue, T., R. Kado, H. Watanabe, J.T. Høeg, K. Inoue, S. Kojima, and B.K.K. Chan. 2013. Influence of water temperature on the larval development of Neoverruca sp. and Ashinkailepas seepiophila—implications for larval dispersal and settlement in the vent and seep environments. Deep-Sea Research I 71:33–37. Yusa, Y., M. Takemura, K. Miyazaki, T. Watanabe, and S. Yamato. 2010. Dwarf males of Octolasmis warwickii of males and hermaphrodites in the suborder Lepadomorpha. Biology Bulletin 218:259–265. Yusa, Y., M. Yoshikawa, J. Kitaura, M. Kawane, Y. Ozaki, S. Yamato, and J.T. Høeg. 2012. Adaptive evolution of sexual systems in pedunculate barnacles. Proceedings of the Royal Society B 279:959–966. Zardus, J., and M. Hadfield. 2004. Larval development and complemental males of Chelonibia testudinaria, a barnacle commensal with sea turtles. Journal of Crustacean Biology 24:409–421.

3 THE TUBE-DWELLING LIFESTYLE IN CRUSTACEANS AND ITS RELATION TO FEEDING

P. Geoffrey Moore and Lucas B. Eastman

The choice of food, the choice of habitation, the construction of dwelling places for themselves or their offspring, methods of defence, methods of attack, are variously carried out by myriads of species. —T.R.R. Stebbing 1871; Essays on Darwinism

Abstract Tube dwelling is an important crustacean lifestyle and is prominent among the Copepoda, Tanaidacea, Amphipoda, Isopoda, and a few Decapoda. This lifestyle has evolved several times in the Crustacea and manifests itself in a variety of morphological adaptations (e.g., elongated habitus, smooth body, thin cuticle, and body flexibility) and tubicolous structures, some of which are constructed by crustaceans themselves (e.g., amphipod silk-based tubes or from shredded algae) and others occupied by these crustaceans but originally built by other organisms. Tubicolous domiciles are often shared with conspecifics or other associated species and are defended because of their importance to their inhabitants for feeding. These crustaceans can be grouped into collectorgatherers, collector-filterers, scrapers, and shredders. Tube homes also serve other functions, such as camouflage and anchorage to the substratum, and provide enhanced filter-feeding efficiency, flexible feeding, emergency rations, secluded mating sites, and protection from predation.

INTRODUCTION Tube dwelling is a lifestyle that has been adopted independently by a broad swath of taxa ranging from diatoms to loricate ciliates (Tintinnidae, Folliculina) and penicillid bivalves (Morton 2004); from sea anemones (Cerianthidae) to several polychaete families (Maldanidae, Terebellidae, Sabellariidae, 35

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding Serpulidae, Sabellidae, Spirorbidae) and particular nemertean worms (McDermott 1988); from some rotifers (Dodson 2006), nematodes (Nehring et al. 1990), and oligochaetes to all phoronids and vestimentiferans, and from some spiders (Segestriidae) to some crustaceans (this chapter). Indeed, the tubicolous lifestyle has a metazoan pedigree stretching back to the Cambrian (Lipps and Signor 1992). The architectural capabilities of terrestrial and freshwater arthropods are well known to specialists and laypersons alike: the naturalist thinking “bees,” “ants,” “termites,” or “caddis larvae” probably automatically conjures up associated images of honeycombs, anthills, termite mounds, and caddis cases. Yet, even to many naturalists—except (hopefully!) aquatic biologists—no such association of ideas would necessarily spring to mind at the mention of “amphipods” or “tanaids,” much less “copepods,” “isopods,” or “decapods.” Indeed, one modern (and otherwise comprehensive) review of the domestic artifacts constructed by the animal kingdom contained no mention of such crustaceans’ domiciliary potentialities (Hansell 1984). More recently, Hansell (2005) made fleeting amends by mentioning some crustaceans’ constructs, although he omitted them from consideration again soon thereafter (Hansell 2007). A much earlier source from Victorian times only alluded in passing to the ischyrocerid amphipod’s structures. Calman’s crustaceologist’s coverage, in 1911, of domicolous behavior in amphipods amounted to but a single paragraph. More recently, in reviewing filter feeding in Crustacea, Grahame (1983) overlooked them entirely. Most surprisingly of all, even Barnard et al. (1991) felt that the literature on tube building in amphipods was “not diverse.” In seeking to redress this (still evident) imbalance of appreciation—as far as crustaceans are concerned at least—the authors derive little solace from the fact that 150 years ago, Spence Bate (1858) likewise sought to bring to the attention of a wider audience the fact that crustaceans (notably amphipods) built nests for temporary or permanent occupation: a plea that clearly fell on deaf ears (adding further weight, were any needed, to Fryer’s plea [1986] for greater historical awareness in biology; Fig. 3.1). The range of domiciles occupied by crustaceans is, in fact, every bit as diverse as those occupied by caddisfly larvae, or caddis worms as they used to be called (see descriptions and illustrations in Miall 1934). Bate (1858) credited the American naturalist Thomas Say with being the first to discover the amphipod Cerapus tubularis (now redefined; see Lowry and Berents 1989) in a tube (illustrated photographically by Ledoyer 1969), although Say believed that the amphipod occupied it only as a tenant. He thought the tube might have been originally constructed by an annelid worm. White (1857), though, was sure that it was “certainly of home manufacture, and not the tube of a zoophyte surreptitiously obtained.” Although Say’s was the first report of a gammaridean in a dwelling, Forskål (1776) had previously illustrated the hyperiid amphipod Phronima sedentaria and its transparent salp barrel. A full appreciation of feeding in tube-dwelling crustaceans, however, requires reference to a wider range of ecological and lifestyle issues. Evolution, functional morphology, social behavior, respiration, reproduction, parasite burden, and predation threat all potentially impact how a particular species goes about food gathering and processing, so such aspects will be touched on here as necessary. Comparisons will also be drawn with studies on tube-dwelling insect larvae (Williams et al. 1987, Armitage et al. 1995). Understandably, most data are about shallow-water species. Sadly, if unsurprisingly, little is known of the wider biology of deep-sea tube-dwelling crustaceans (e.g., Hassack and Holdich 1987, Bird and Holdich 1989a). Terminology Here, we define what constitutes a tube in this particular context. We have excluded burrowing species in this chapter, although they live in a tubular-form domicile, because those crustaceans are documented elsewhere in this volume (see Chapter  4 in this volume) and despite some authors working on burrowing mud shrimps referring to them as tube-dwelling (Stamhuis and Videler



P. Geoffrey Moore and Lucas B. Eastman

A

B

Fig. 3.1. (A) Tubes of Podocerus fucicola on Ulva and Tubularia. (B)  Tube of Ampithoe rubricata at the holdfast of Laminaria. Modified from Bate (1858).

1998). Similarly, the “tubicolous” isopod Excirolana kumari of Bowman (1971) is actually a digger. A continuum exists, though, between tube-dwelling and burrowing lifestyles that is evident where sediments are involved, even within closely related species (see also Schäfer 1972), so it is appropriate not to be too proscriptive of coverage. For instance, the “tube-builder” Crassicorophium bonnellii is capable of burrowing (Shillaker and Moore 1978), whereas the “burrower” Corophium volutator is capable of tube building (Meadows and Reid 1966). Wood- or kelp-boring crustaceans are dealt with in Chapter  5 in this volume. In delving into tube-dwelling lifestyles, however, those crustaceans too merit occasional asides here. Tube-dwelling propensity and tube-building ability should not be confused; they are not necessarily the same thing. “Tubicolous” generally means living in a self-constructed tube, but some crustaceans secondarily occupy the tubes of other organisms; in this chapter, these are also considered to be tubicolous.

CRUSTACEAN TAXA INVOLVED IN TUBE DWELLING Copepoda Harpacticoidea Tube building has been reported in Stenhelia (Delavalia) palustris and Pseudostenhelia wellsi (William-Howze and Fleeger 1987, Chandler and Fleeger 1984), the presence of which can facilitate colonization by other species (Chandler and Fleeger 1987). Dactylopusia tisboides constructs

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding mucous tubes (Peachey and Bell 1997). Diarthrodes nobilis produces copious mucus to construct a mucus bag on the thallus of algae, which is then used as a house and a food trap (Hicks and Grahame 1979). A congener, D. cystoecus, produces galls, as well as encapsulating mucus, to protect the copepod from dislodgement (Fahrenbach 1962). A number of thalestrid harpacticoids have been described as burrowing or mining into algae either as nauplii or as adults (for references, see Ho and Hong 1988). Many copepods live in tubes made by other invertebrates. Thus, cyclopoids of the families Serpulidicolidae and Sabelliphilidae are associates of tubicolous polychaetes (Stock 1979, Kim 2006). Peracarida Amphipoda Among the gammaridean Amphipoda, a tubicolous or nesting life strategy is associated mainly with “corophioid” and “ampeliscoid” species (Lakshmana Rao and Shyamasundari 1963, Moore and Myers 1988, Myers and Lowry 2003). Recently, however, Martin and Davis (2001) have advocated the abandonment of the superfamily concept in amphipods in favor of dealing with them at the family level until trustworthy cladistic analysis provides a more reliable higher systematic framework. Myers and Lowry (2003), however, have generated a new classification of the suborder Corophiidea based on cladistic methodology. Not all corophiideans, however, are tube-dwellers. Fabrication of dwellings is very typical within the Aoridae, Neomegamphopidae, Isaeidae, Photidae, Corophiidae, and Ischyroceridae, although it seems to be universal within the Ampeliscidae. Podocerus, for instance, lacks silk-spinning glands (Barnard et al. 1988). Some dulichiid amphipods construct sediment rods or whips (Laubitz 1977, Moore and Earll 1985, Mattson and Cedhagen 1989, Thiel 1997a, Thiel et al. 1997), which may be derivative from a corophiidean tube-building ancestry (Dixon and Moore 1997). The ancestral corophiid is a tube-dweller with normal mouthparts, but biancolins and chelurids have lost the tube-spinning glands and developed kelp- and wood-boring mechanisms (Barnard 1974). According to Bousfield (personal communication to PGM), some lysianassid relatives may be involved in tube dwelling, too (“Conicostomatidae” [our quotes] and allies). Just (1977a) has described Pterunciola spinipes living in pteropod shells. Tritaeta gibbosa forms vesicles on the outside of sponges ( Jones et al. 1973), but dexaminids do not construct actual tubes. The bulk of this review is inevitably about amphipods because more is known about their tubicolous habits. Barnard et  al. (1991) classified tube building in amphipods into 12 kinds, with many subdivisions. Isopoda Although isopods are not known to build tubes for themselves (Tanaka and Nishi 2008), the little-known vermiform flabelliferan isopod Eisothistos vermiformis, from Australia, occupies the tube of Vermilia sp. (Polychaeta:  Serpulidae) mimicking its appearance uncannily (Stebbing 1893). It has been suggested plausibly that the tail of the equally elongated Anthura gracilis might mimic the crown of the polychaete Sabellaria spinulosa, since one female A. gracilis was dredged off Plymouth and retrieved head inward in a tube of this worm (Sexton 1914). Poore and Lew Ton (1990) regarded the semicylindrical body plan of certain valviferan isopods as evidence suggestive of tube dwelling. Garstang (1892) observed Zenobiana prismatica (as Idotea parallela) inhabiting a piece of the stem of a dead Zostera plant, which it carried about with it “like a caddis-worm in its tube.”

P. Geoffrey Moore and Lucas B. Eastman

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Fig. 3.2. Tubes built by various tanaids. Modified from Hassack and Holdich (1987), obtained with permission from John Wiley and Sons. (A) Collettea cylindrata tube inside a pteropod shell. (B) Typhlotanais aequiremis tube with tanaid inside. (C) Typhlotanais spinicauda tube. (D) Typhlotanais sp. H13 tube (see Hassack and Holdich for details regarding this species). (E) Typhlotanais sp. H20 tube (see Hassack and Holdich for details regarding this species). (F–I) Scanning electron micrographs of tanaid tubes. (F) Typhlotanais sp. H20 tube. Scale = 170 µm. (G) Anterior end of Typhlotanais sp. H20 tube showing its well-developed cylindrical form. Scale = 33 µm. (H) Surface view of Typhlotanais sp. H13 tube showing random arrangement of spicules. Scale = 100 µm. (I) Detail of Typhlotanais sp. H13 spicules. Scale = 10 µm. See text for details regarding these species.

Tanaidacea Tanaids may be tube dwelling, burrowing, or free-living (Fig. 3.2; Greve 1967, Johnson 1982, Holdich and Jones 1983, Bird and Holdich 1989a, Kudinova-Pasternak 1991, Lewis 1998, Larsen 2005). Note that Issel’s tubicolous “isopod” (1912), Z. prismatica, is a tanaid. Although many reference works state that tanaids are largely tubicolous, a review of the literature reveals that the domicolous habit has been taken up by relatively few tanaid genera (Hassack and Holdich 1987). Such a habit, creating a place to live, mate, and/or brood the young, is restricted to a few genera in the suborder Tanaidomorpha: Allotanais, Langitanais, Parasinelobus, Sinelobus, Tanais, Haplocope, Leptognathia, Nematotanais, Typhlotanais, Anarthruropsis, Heterotanais, and Leptochelia (see table 1 in Hassack and Holdich 1987). Hassack and Holdich (1987) reckoned that there were no tube builders amongst the Apseudomorpha (but note Larsen 2005) and Neotanaidomorpha. Larsen (2005) has recently provided an excellent summary of the literature on this subject. Decapoda Most domicolous decapod crustaceans live in burrows rather than in tubes (see Chapter 4 in this volume), even if some species may extend burrow entrances into “chimneys” (Shih et al. 2005). We have elected to exclude hermit crabs from consideration herein, although the less well-known

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding amphipod Photis conchicola—a hermit crab analogue—deserves mention (Carter 1982; see also Gauthier 1941). The “unconventional” hermit crab Discorsopagurus schmitti may occupy a number of microhabitats ranging from spiral gastropod shells, straight tusk shells, and worm tubes (Gherardi and McLaughlin 1995, Gherardi 1996, Gherardi 2004). The decapods Polyonyx (Galatheidae) and Pinnixa (Pinnotheridae) filter feed inside the parchment tubes of the polychaete Chaetopterus (Pearse 1913).

EVOLUTION OF TUBICOLOUS HABITS Living in tubes has evolved several times among the Crustacea. The universality of the opposed orientation of the thoracopods (pereopods P3 and P4 vs. P5, P6, and P7) of gammaridean amphipods betokens a plesiomorphic condition consistent with a clinging lifestyle being primitive (Steele 1988). On this view, tube building would be regarded as a specialist, derived condition. An alternative scenario, expounded by Barnard and Barnard (1983) proposed that the construction of abodes by amphipods (their attention being focused on their concept of the Corophioidea) is ancestral, a trait that has been secondarily lost in other amphipods; “the early amphipods could easily have been domicolous and then have radiated into nestlers lacking the spinning glands used to weave the abode” (Barnard and Barnard 1983, Borowsky 1984). In the absence of hard (fossil) evidence, the inferred polarity of any proposed amphipod lineages may always be contentious, making amphipod phylogeny something of an armchair science. Alan Myers and Jim Lowry, however, are slowly resolving issues of amphipod phylogeny using cladistic approaches. Although prepared to be convinced otherwise, these authors favor the view that silk production and abode construction by amphipods be regarded as derivative. Based on a cladistic analysis of the Corophiidea, Myers and Lowry (2003) regard the glandular pereopods of corophiideans as “a major evolutionary innovation.” Bate and Westwood (1863) had wondered how amphipods like Ampithoe rubricata made the threads that held their nest together. Smith (1874) drew attention to the glandular pereopods (P3 and P4) of certain Amphipoda and associated those features, together with the dactylar pore, with tube-building ability (Fig. 3.3; Della Valle 1893, Goodhart 1939, Barnard and Barnard 1983, Myers and Lowry 2003, Kronenberger et al. 2012a,b). In amphipods, the main glandular mass resides in the merus of P3 and P4 in ampeliscids (and in Aetiopedes) but in their bases in “corophioids” (Moore and Myers 1988; note that Aetiopedes was regarded as a hadziid by Bousfield and Shih [1994] but is now classified within the caprellidan clade by Myers and Lowry [2003]). Goodhart (1939) considered that the dermal glands, scattered all over the body of Leptocheirus pilosus, probably secreted mucous cement. Interestingly, Shyamasundari and Hanumantha Rao (1974) have also described mucus-secreting glands in the appendages (antennules, antennae, pereopods, and uropods) of some free-living talitrid amphipods. Tanaid tubes consist of a mucoid tubular structure formed from secretions of glands situated in the pereonal cavity close to its junction with the cephalothorax. The latter open via pores onto the dactyli of the first pair of pereopods (Hassack and Holdich 1987). In tanaids (Larsen 2005), glands in Tanapseudes gutui are situated in P3–P5 (but lack an outlet on the pereopods, so are unlikely to be involved in tube construction), not in P1–P3, as in the Tanaidomorpha, and hence are not homologous. P2 is only the “spinning leg” in Tanais dulongii (= T. cavolinii) and is not involved in locomotion ( Johnson and Attramadal 1982a). Tegumental glands (see Holdich and Jones 1983) can be seen especially well in some species of Typhlotanais, the archetypal tube builders, according to Graham Bird (personal communication to PGM). There seem to be no obvious means for producing tube mucus in most apseudomorphans; however, Kalliapseudes has been reported building tubes in the laboratory (Larsen 2005). Tanais dulongii (=. T. cavolinii) spins an anchor thread that functions as a lifeline in exposed habitats ( Johnson and Attramadal 1982a).



P. Geoffrey Moore and Lucas B. Eastman

A

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Fig. 3.3. Confocal and scanning electron micrographs illustrating amphipod, tube, and details of amphipod silk fibers. From Kronenberger et al. (2012a), obtained with permission from Springer. See color version of this figure in the centerfold. (A) Confocal micrograph of Crassicorophium bonnellii stained with carmine. Arrows indicate two of four secretory legs (p3 and p4) involved in secreting and spinning amphipod silk; scale bar is 500 μm. (B) Illustration showing C. bonnellii inhabiting its tube, holding a sand grain with its antennae and gnathopods; scale bar is 500 μm. (C) Scanning electron micrograph showing a typical open-ended amphipod tube; scale bar is 500 μm. (D) Scanning electron micrograph showing a net of C. bonnellii silk fibers spun to cement the tube’s sand grains together; scale bar is 50 μm. (E) Scanning electron micrograph illustrating the silk net in more details; scale bar is 10 μm. (F) Scanning electron micrograph showing detail of silk fibers; scale bar is 1 μm.

The precise evolutionary derivation of silk-producing glands in crustaceans remains to be established. It may be significant, however, that tegumental glands have been described for a wide variety of primitive and advanced crustaceans ranging from mystacocarids (Pochon-Masson et al. 1975), to copepods (Mauchline 1977, Mauchline and Nemoto 1977, Williams-Howze and Fleeger 1987, Williams-Howze et al. 1987), thalassinids (Dworschak 1998), and terrestrial isopods

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding (Gorvett 1956; see Yonge 1932, Thomas 1944, Hipeau-Jacquotte 1987 for further references). Not all epidermal glands are concerned with cuticle formation (Walley 1967). In the harpacticoid copepod Pseudostenhelia, mucus is apparently produced from the ventrolateral margin of the cephalothorax (Chandler and Fleeger 1984). The fact that in such glands the secretory products are transported to the exterior through a cuticularized canal and secreted by the canal cell (Hipeau-Jacquotte 1987, Halcrow 1988), provides the necessary essentials for evolution to refine. In addition, mucus-secreting glands have been described in the anterior alimentary canal of crustaceans (Walley 1967, Shyamasundari and Hanumantha Rao 1977)  associated perhaps with lubricating or binding food particles. Gene switching mechanisms (yet to be identified) would provide a putative means for concentration of silk-producing glands in favorable body locations. The trend that specialization is often accompanied by a reduction in the number of serially reiterated structures (Williston’s Law), as revealed in the evolution of insect wing number (Carroll 2005), furnishes us with a useful paradigm. Changes in Hox gene expression patterns have been revealed to be important in trunk tagmatization of the isopod Porcellio scaber (cf. insects) by Abzhanov and Kaufman (2000; note also Deutsch and Mouchel-Vielh [2003]). Nurture as well as nature clearly has a role to play in the evo-devo of tube-dwelling crustaceans. Thus, the work of Gherardi and McLaughlin (1995) on the juvenile development of the hermit crab D. schmitti has demonstrated that whereas microhabitats do not control pleopod loss, the use of a worm tube as a microhabitat (as opposed to a spiral gastropod shell or a straight tusk shell) does at least influence positioning of the uropods. To conjecture, an ancestor of the domicolous, silk-spinning Amphipoda may have evolved from a species that had adopted a body-covering habit like that described by Just (1981) for the synopiid Tiron bellairsi, involving carriage of protective slabs of coral debris held in place by pincer-like pereopod dactyls (cf. also Gray and Barnard 1970). The nature of the amphipod silks produced by C. bonnellii and Lembos websteri has been investigated by Shillaker (1977, see also Shillaker and Moore 1978) and, more recently, by Kronenberger et al. (2012a,b). They have been shown to contain mucopolysaccharides and proteins. The ability to produce sticky material (necessary to provide the glue for domicile construction) in such different crustacean lineages as the Amphipoda, Tanaidacea, and Copepoda must be regarded as convergent evolution in response to selective pressures, most probably involving several factors including a reduced likelihood of predation (Nelson 1979; note DeWitt and Levinton 1985, Cuker et al. 1992; cf. Sommer 1997 on tube-dwelling diatoms). Interestingly, Hansell (2005) claimed that the role of mucus in home building by animals is fairly limited. Clearly, crustaceans represent an exception to this general rule.

TUBE STRUCTURES AND FUNCTIONAL MORPHOLOGY OF OCCUPANTS Domiciles, including tubes, are made from a variety of materials:  silt and sand grains, foraminiferan tests, algal fragments, echinoid spines, and the like (Bate and Westwood 1863, Hart 1930, Enequist 1949, Johnson and Attramadal 1982a, Chandler and Fleeger 1984, Hassack and Holdich 1987, Barnard et al. 1988, Ortiz 2001, Appadoo and Myers 2003, Myers and Lowry 2003, Larsen 2005)  cemented together and typically lined with silk (White 1857, Shillaker and Moore 1978, Appadoo and Myers 2003, Myers and Lowry 2003). Microdeutopus gryllotalpa will incorporate almost anything into their tubes, including glass beads or shed exuvia (Myers, personal communication to PGM). The tube of C. tubularis has been characterized as being of “leathery” texture (Morino 1976). Mills (1967b) described the tubes of Ampelisca abdita as composed of a “grey, non-chitinous, parchment-like material and fine sand grains” (p.305). Lowry and Berents (2005) illustrated new Cerapus species from Australia and Papua New Guinea with tubes that were



P. Geoffrey Moore and Lucas B. Eastman

“wrapped and parchment-like and sometimes elaborately covered with pieces of cut algae and seagrasses” (p.153). Barnard et al. (1991) refer to Grandidierella bonnieroides and a Cerapus species commencing tube formation “by enrolling themselves in a blanket of detritus and gluing clumps of the material with strands of silk in a few minutes” (p.239). In the laboratory, some amphipod species will build silk-only tubes in the absence of sediment, for example, Corophium spp. (Shillaker 1977, Barnard et al. 1988, PGM personal observation): others, for example, Grandidierella sp. (bonnieroides), will not (Barnard et al. 1988). Typically, tubes exceed, and are a function of (Shillaker and Moore 1978), the body length of the occupant in Amphipoda (Mills 1967b, Barnard et  al. 1991, Dixon and Moore 1997, Appadoo and Myers 2003; cf. Hassack and Holdich 1987 on tanaids). Their walls are flexible, which assists the animal maneuvering inside (Mills 1967b). Lincoln (1979) summarized the situation for British amphipod species thus:  [T]‌he domiciles may be delicate tubes resting on the sediment surface (Ampelisca, Byblis, Haploops), fibrous tubes or nests in algal, hydroid, or other growths (Jassa, Parajassa), loose retreats attached to rocks, stones or algae formed from shore debris (Ampithoe), or more perfectly sculptured cylindrical or conical tubes which may be flexible and membraneous (Cerapus, Ericthonius), parchment-like (Siphonoecetes), or formed from mud (Cerapus crassicornis), or small fragments of shells or tiny pebbles (Siphonoecetes typicus). Corophium species make “U”-shaped burrows in sandy and muddy sediments, Chelura terebrans burrows into submerged or waterlogged timber and Amphitholina cuniculus makes its burrows in kelp stems (Alaria). Schäfer (1972) described Siphonoecetes coletti as living in tubes of consolidated shell fragments, small pebbles, and fine spines of sea urchins. Lowry and Berents (1996) illustrated a variety of tubes made by members of the Ericthonius group (note also Ledoyer [1969] on E. pugnax), but Dixon and Moore (1997) found that E. punctatus has an architecturally distinctive tube in that it tapered along its length (cf. Zavattari 1920 on E. brasiliensis), having an unusual oblique main entrance at its widest end. In an earlier paper, Lowry and Berents (1989) described the tube of C. tubularis as being composed of fine sediment laid down in concentric rings. Mills (1967b) has described the different phases of construction involved during tube building in A. abdita and noted that very fine particles were used finally on the outside of the (laterally flattened) tube. Like those of C. bonnellii, the tube entrances of another amphipod, L. pilosus, are smaller than the bore at the tube’s mid-point (Goodhart 1939, Dixon and Moore 1997). Meadows (1967) found that the amphipod C.  volutator selected small grains for building its tube. Prathep et al. (2003) noted that the abundance of the tanaid T. dulongii was strongly associated with the relative abundance of the sediment fraction (250–500 µm) that it uses to build its tube. Johnson and Attramadal (1982a) pointed out that sedimented small particles are scarce in that species’ exposed habitat. More detailed information about tube structure in different crustaceans is still needed, on a par with that available for polychaetes (see Vovelle 1973 and Rees 1976 for further references). Some amphipods are less selective of tube-building materials (e.g., Corophium insidiosum) than others (e.g., Jassa falcata): the latter species utilizes sand grains to only a very limited extent (Ulrich et al. 1995). Some tanaids also are selective in their choice of tube-building materials, while others use indiscriminately whatever is available ( Johnson and Attramadal 1982a, Hassack and Holdich 1987). Males construct real tubes in the Tanaidae, albeit shorter and less well maintained than those of the female. Thomas and Heard (1979) described the amphipod Cerapus benthophilus constructing conspicuous mats or “tufts” of interwoven tubes in shallow water. Shillaker and Moore (1978) described C. bonnellii building mats away from solid surfaces (something that L. websteri never did;

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding cf. Matsumasa 1994). In appropriate circumstances of sand availability, it could construct a veritable honeycomb of tubes, filling in the spaces between kelp haptera. The tanaidacean Parasinelobus chevreuxi lives in littoral, crevice-based “colonies” of long, fixed interconnecting tubes (Holdich and Jones 1983). The harpacticoid copepod P.  wellsi also builds extensive networks of mucus tubes (Chandler and Fleeger 1987). Amphipod abode complexes (as in Siphonoecetes dellavallei and Bubocorophium tanabensis) have been described: in the former species, males catch up to three females with abodes and glue them to the sides of their own house (Richter 1978b, Just 1988). The quest for a eusocial marine crustacean (Spanier et al. 1993, Duffy and Macdonald 1999) has culminated in Duffy’s work on alpheid shrimps (Duffy 2007). Alexander et al. (1991) proposed that extended parental care and occupation of particular microhabitats or nests that are safe, provide food, and are expandable, are common conditions for the evolution of eusociality. In order to also ensure the longevity of the nest, but still be able to feed directly on their nest, Peramphithoe femorata exploits the growth pattern of the kelp blades Macrocystis pyrifera, which grow from the basal growth meristem, by building its nest near the distal-most part of the blades. Thus, as the blade grows and the amphipod feeds on its nest, the amphipod continues to construct its nest with blade material provided from the basal growth meristem, so that its nest advances toward the blade base (Cerda et al. 2010). Gutow et al. (2012) found that the mortality of the tethered amphipods P. femorata on the thalli of kelp M. pyrifera was mitigated by nests that the amphipods formed from the blades. The location along the thalli of M. pyrifera that the amphipods chose to occupy and build their nests was suggested to maximize their survival. In the upper parts of the kelp (the majority of amphipods were located in the upper 40% of the stipes), the amphipods were relatively safe from benthic predators due to the dense kelp forest canopy (Gutow et al. 2012). Abode complexes among domicolous Amphipoda thus merit further ethological attention (cf. Atkinson et al. 1982 on the communally burrowing Maera loveni; Ortiz 2001 on the interconnecting galleries of G. bonnieroides). Adults of the amphipod Cymadusa filosa built an average of four tubes over a 15-day period, and there was a strong relationship between body length and tube length in both male and females (Fig. 3.4; Appadoo and Myers 2003). Shillaker and Moore (1978) reported that C. bonnellii builds a covering tube in less than 15 min (so important is the creation of its refuge). Grandidierella bonnieroides fabricated tubes in 2–4 h (Ortiz 2001). Tubicolous harpacticoids also construct tubes speedily, in 1–2 h (Chandler and Fleeger 1984). Infaunal tube-building amphipods (Ampeliscidae, Leptocheirus, Unciola) construct tubes in the substratum with one end open at the surface (Bousfield 1973). Goodhart (1941), however, reported L. pilosus living in tubes built against the flat surface of stones or on the thallus of the rhodophyte Chondrus crispus. The discoid domiciliary cases of the South African amphipod Ampelisca excavata, composed of fine-grained sand, have been described by Gray and Barnard (1970). The animal lives tightly curled inside its case, with the head and antennae visible through a narrow, slit-like opening. The cases themselves were taken from inside cirripede burrows on the gastropod Turbo sarmaticus. Some tanaids invariably build tubes open at both ends (Holdich and Jones 1983), whereas in other species the female builds tubes only open at the front end, while the male keeps the tube open at both ends ( Johnson and Attramadal 1982a, Larsen 2005). For brooding purposes, the tube may even be closed at both ends; for example, in the tanaid Heterotanais oerstedi (Hassack and Holdich 1987). Some tubicolous tanaids use their tube for extramarsupial brooding (Hassack and Holdich 1987), analogous to the hyperiid amphipod Phronima within salp barrels. The gammaridean amphipod Haploops vallifera also broods its young in the tube: the females, most unusually, do not possess oostegites (Dauvin 1996). The tanaidacean Hexapleomera robusta even builds tubes adhering to the skin of the Caribbean manatee (Trichechus manatus manatus), mainly along the backbone depression and, in some instances, associated with clusters of barnacles. This tanaid is presumed to capture food particles disturbed by the manatee feeding (Morales-Vela et al. 2008).



P. Geoffrey Moore and Lucas B. Eastman

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Fig. 3.4. (A) Cymadusa filosa specimens in stock aquarium constructing tubes by folding Ulva lactuca thalli. Speckles indicate sand particles or detritus. Scale bar = 5 mm. (B) Relationship between body length and tube length in males of C. filosa (log y = 0.593 + 0.0579×, F(2, 186) = 76.66, P < 0.0001, number of observations = 188). (C) Relationship between body length and tube length in females of C. filosa (log y = 0.759 + 0.043×, F(2, 160)  =  37.52, P < 0.0001, number of observations  =  162). From Appadoo and Myers (2003), obtained with permission from Taylor & Francis.

The adaptive significance of an elongated cylindrical body shape to animals living within tubes has already been mentioned (note Poore and Lew Ton 1990). Morphological adaptations are most visible at either end of a tube-dweller’s body, involving the head, gnathopods and urosome (Myers and Lowry 2003). Conlan (1983) has commented on this from the perspective of the photid amphipods. Thus, the long and densely setose antennae of Gammaropsis, Podoceropsis and Photis would extend the range for collection of sensory information while the lengthened ocular lobes would increase the ability to see from the tube aperture by a slight margin. The opposite strategy, highly developed in the Corophiidae, is visible in Protomedeia and Cheirimedeia where the second antennae shorten and thicken for food gathering. (p.1; note also Barnard 1958b on Gaviota, Dixon and Moore 1997 on Ericthonius punctatus, Myers and Lowry 2003 on corophiideans in general) Genera like Corophium, Leptocheirus, Haplocheira, Kuphocheira, Anonychocheirus, Bemlos (some), Microdeutopus, and Autonoe with highly setose gnathopodal filtering fans, are adapted for filter feeding (Goodhart 1939, Moore and Myers 1983, Dixon and Moore 1997). At the other end of the body, the urosome (uropod 3 in Photis, telson in Ampithoe and Sunamphitoe) may be equipped with hooks to allow the animal to retain a purchase on the mouth of the tube during partial emergence to gather food items from its immediate vicinity. The fleshy “corophioid” telson may be reflective of an enhanced muscularity adaptive in terms of helping to maintain a grip on the mouth of the tube during incomplete emergence or in plugging the rear entrance of the tube when the animal is active at the other end (Bousfield and Hoover 1997). Sars (1895)

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding regarded the widened peduncular article of the first antenna in Cerapus crassicornis as acting as an operculum occluding its tube opening at the head end. Having abandoned tube dwelling, the redundant urosome in the highly derived epifaunal caprellids (Laubitz 1977) was reduced to a vestige (Myers and Lowry 2003). The elongation of pereonites in males and in females of cerapid species appear to be independent evolutionary events. These and associated character states appear to be modifications for accommodating, within the tube, the massive gnathopod 2 that develops in mature males (Lowry and Berents 1989). In hyperadult males of Aora gracilis, the massive first gnathopod (dominant in aorids) can severely impair access to the mouthparts by the second pair (Dixon and Moore 1997). The ischyrocerid habit of externalizing food gathering at the tube entrance (Connell 1963, Nair and Anger 1979b, Dixon and Moore 1997) might be regarded as one step along the line leading to clinging, rod-building podocerid types (Laubitz 1983, Dixon and Moore 1997). No known amphipods use silk to manufacture a trap for live prey (cf. spiders) or to spin mucous nets to passively trap seston particles (in the manner of net-spinning caddis worms in fresh water [Walshe 1951, Alstad  1987] or of some marine polychaetes and echiurans). Crassicorophium bonnellii, however, has been reported capturing and consuming barnacle cyprid larvae while feeding on seston using the filtering setae of the second gnathopods (Dixon and Moore 1997). These authors noted that food particles also become entrapped without using this filter. A couple of species of tanaids, however, have been reported to spin a meshwork of strands extending from the front end of the tube; these function as detectors of interlopers or possible prey (Bückle-Ramirez 1965), in the manner of a spider’s web (Larsen 2005). In a sense, though, marine filter-feeding malacostracans that deploy setose filter funnels (associated with setose anterior thoracopods) across the current inside tubes occupy analogous niches to net-spinning caddisfly larvae in fresh waters. Moss (1980) has highlighted other such trophic parallels between organisms from disparate groups between these major aquatic habitats (e.g., as between chaetognaths and Chaoborus midge larvae, or between salps and daphnids). There are only so many ways to intercept active prey or suspended food particles (Wotton 1994), and it should not be surprising that aquatic organisms have risen to these challenges in parallel ways over evolutionary time.

TYPES OF ARTIFACTS CONSTRUCTED OR OCCUPIED BY CRUSTACEANS There is a continuous spectrum of domiciles constructed by crustaceans with lifestyles ranging from nesting and tube building, to tunnelling and rod (or whip) building. The size and shape of these domiciles varies according to the situation and purpose of the construction. Artifacts may be built de novo or utilized secondarily. Thus, nesting species may take over empty mollusk shells (Gherardi and McLaughlin 1995, Larsen 2005) or worm tubes (Gherardi and McLaughlin 1995)  or manipulate algal fronds (Skutch 1926, Griffiths 1979, Conlan 1982, Poore and Lowry 1997). In particular, Myers and Lowry (2003) noted that, among the corophiid Amphipoda, the Siphonoecetes-group often uses empty shells of other organisms such as gastropods, scaphopods, or polychaetes (see also Richter 1978b). Considerable descriptive work on these species has been done by Just (1983, 1984a,b, 1985, 1987) who, in 1988, summarized the early work on the group (note also Stebbing 1893). Although unable to build tubes themselves, podocerids will nevertheless occupy tubes produced and vacated by tube-building corophiideans (Barnard et al. 1988), indicative of their domicolous ancestry (Myers and Lowry 2003). There are analogies here with the secondary occupation of tubes and burrows in the sea bed; as by the amphipod Podocerus, which will capture empty tubes of other taxa (including other phyla; Barnard et al. 1988) or by the galatheid Munida



P. Geoffrey Moore and Lucas B. Eastman

rugosa, which will occupy abandoned Cepola rubescens (red bandfish) burrows (Atkinson et  al. 1977). Griffiths (personal communication to PGM) also reported that A.  excavata, a South African species, occupies old cirripede tubes (possibly ascothoracids) in gastropod shells. Mills (1967b) has described the tube-building activity of A. abdita (see also Wildish and Kristmanson 1997). Many liljeborgiids live in tubes, usually ones that have been constructed by worms, shrimps, or other organisms. Some urothoids (e.g., Cunicus) apparently attach sand grains to their posterior (urosome), an action that suggests they may be living in sand tubes (Bousfield, personal communication to PGM). PGM has also noted many times that Dexamine thea is often found with sand grains sticking to its rugose cuticle. Many of the Dexaminoidea are nestlers, close to house-builders (especially Polycheria; note Skogsberg and Vansell 1928), and the talitroidean Najnidae burrow into kelp stipes that react by forming galls around them (note also Conlan 2007 on Alatajassa). Tube-building behavior differs between genera of ampithoid amphipods: Ampithoe caddi, A. kava, and A. ngana build tubes on the surface of macroalgae or between neighboring blades, with added detritus, algal fragments, and fecal pellets (Poore and Lowry 1997; cf. also Holmes 1901, Skutch 1926, Heller 1968 on A. longimana, A. rubricata, and A. lacertosa, respectively). Pseudamphithoides inhabits domiciles constructed from pieces of algae, which it cuts and binds together (Lewis and Kensley 1982, see also Just 1977b on Pseudamphithoides; see Jones et al. 1973, Williams-Howze and Fleeger 1987; Fig. 3.5). Peramphithoe curls algal blades into a tube or cements neighboring blades together to form an enclosed nest in a fashion similar to that of other species in this genus (Conlan 1982, Poore and Lowry 1997). Other ampithoids, for example, Amphitholina (Myers 1974), burrow into the stipes of kelps, very detrimentally in the case of Peramphithoe (Conlan and Chess 1992, Chess 1993). Although members of the Amphipoda Hyperiidea inhabit barrels, these are not solely of their own construction. They modify the transparent tests of gelatinous zooplankton, such as siphonophores, salps, and pyrosomas (Madin and Harbison 1977, Nishikawa et al. 2005). Interestingly, it has been suggested that these amphipods may exhibit subsocial behavior (Spanier et al. 1993).

TUBES AS SHARED RESOURCES Hamond (1967) reported that hundreds of C. bonnellii were found “apparently sharing the tubes of Ampelisca tenuicornis with the owners themselves” (p.113). It is a well-known fact that many tubicolous polychaetes find themselves sharing their tubes with other commensals, scaleworms in particular (with often quite specific commensal relationships having evolved; see Marine Biological Association 1957, Zühlke 2001). The same is true among the tubicolous Crustacea. After all, metazoan tubes have been around since the Cambrian (Lipps and Signor 1992), and there has been no shortage of time for many evolutionary lines to exploit these protected microhabitats and for mutualistic, commensal, or parasitic associations to co-evolve. Thus, the harpacticoid copepod Parasunaristes chelicerata lives within domiciles constructed by the amphipod Siphonoecetes sp. in the northern Red Sea (Falck and Bowman 1994). It is interesting that the brood-pouch parasitic copepod Sphaeronella leuckartii was so prevalent in tubicolous amphipod species A.  gracilis in Lough Hyne, Ireland (Costello and Myers 1989), although this copepod genus infects a wide range of amphipods. Bunched together tubicolous species may be particularly vulnerable. That said, Sheader (1977) reported only low infestations of S. longipes in A. tenuicornis. Hamond (2002) speculated that the long-lasting burrows in thick durable clay at Holme, Norfolk, provide excellent shelter for nicothoid larvae, so that a Corophium meeting a larva would be highly likely to be infected. Escobar-Briones et al. (1999) noted that feeding on sediment by a tubicolous tanaid (Discapseudes holthuisi) made it vulnerable to the ingestion of acanthocephalan eggs. The influence

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding

A

B

D

C

E 2 mm

Fig. 3.5. Sequence of algal pod construction by Pseudamphithoides incurvaria on Dictyota bartayresii. From Lewis and Kensley (1982), obtained with permission from Taylor & Francis. (A) Initiation of cut and notch: branch tip will form first valve. (B) Continuation of cut-across algal thallus. (C) Measuring and clearing “algal hairs” off second branch tip. (D) Second valve being cut. (E) Completed pod with valves attached along margins by threadlike secretions.

that parasite or epibiont burden may have on feeding requirements or ability of tubicolous crustaceans has not been studied in any depth (note Boxshall and Lincoln 1987 on Tantulocarida; cf. Rankin and Bonilla-Naar 1946 on polychaetes), but it has been shown that there is a positive correlation between trematode infestation intensity and metabolic heat loss in C. volutator (Meissner and Schaarschmidt 2000). The parasite specificity of benthic crustaceans (including tube-dwelling amphipods) is reportedly low in the Baltic (Kesting et al. 1996). However, a neorhabdocoelan turbellarian (Kronbergia amphipodicola) infects the body cavity of A. macrocephala, A. tenuicornis, and Haploops tenuis (but not H. tubicola) in the Øresund, causing sterility and eventual death of the host (Christensen and Kanneworff 1965). It is interesting, then, how different the parasite burdens of two closely related (congeneric) and coexisting tubicolous amphipod species proved to be in the Øresund (note Christensen and Kanneworff 1965, Kanneworff 1966 on Haploops; cf. also Moore 1981a, Jensen et  al. 1998). McCurdy et  al. (1999) provided evidence that the parasitic nematode



P. Geoffrey Moore and Lucas B. Eastman

Skrjabinoclava manipulates host Corophium behavior to increase transmission to the sandpiper Calidris pusilla. Precopulatory mate guarding (amplexus) is a feature of free-living gammarid amphipods, but mate guarding is achieved by attendance in tube-dwelling amphipods (Conlan 2004). Males and females—often with the female being larger than the male (cf. amplexing species; Moore 1981a)—may then be found tube sharing (Fig. 3.6; Chapman and Dorman 1975, Fish and Fish 1989, Appadoo and Myers 2003). Dr. Betty Borowsky (personal communication to PGM) stated that she knows “for sure that a tube is a critical requirement for the expression of reproductive behaviors [in the amphipod M. gryllotalpa], because males will not express courtship or mating unless both the male and female are at least partially inside the same tube.” In general, however, each animal lives alone in its tube and defends it against conspecifics. Immediately prior to a female’s molt, this behavior changes, and the female permits a male to enter and share the tube. The possession of stridulating ridges in the amphipod Photis may serve in communication and sexual attraction (Conlan 1983, 1994; note Stephensen 1938 on Grandidierella japonica,

Fig. 3.6. Cymadusa filosa male and female sharing a tube made by folding Ulva lactuca; scale bar = 2 mm. From Appadoo and Myers (2003), obtained with permission from Taylor & Francis.

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding Myers and McGrath 1984 on some species of Ericthonius), supplementing the usual pheromonal signals emanating from a molting female (Borowsky et  al. 1987). Tube sharing in amphipods continues until the female molts, when copulation occurs (Borowsky 1991). Copulation normally takes place within minutes or 1–2 h of the female molting (Moore 1981a, Prince William Sound Regional Citizens’ Advisory Council 2004). Feeding ceases at the molt, a process that may be repeated in shallow-water amphipods in temperate seas with a semilunar periodicity at summer temperatures (Fish and Mills 1979, Moore 1981a, McCurdy et al. 2003). Residential tubes of receptive females of the amphipod M. gryllotalpa stimulate pair formation (Borowsky 1989). Nests of Exampithoe kutti may be shared among a male, a female, and their offspring, or combinations thereof (Poore and Lowry 1997). This habit is similar to that of the burrowing species Peramphithoe stypotrupes, in which the offspring coexist in a burrow with their parents (Conlan and Chess 1992). Emergent juveniles are responsible for short-distance dispersal (Prince William Sound Regional Citizens’ Advisory Council 2004, Havermans et al. 2007), although adults of some species might indulge in pelagic swimming or epibenthic crawling as well (Fish and Mills 1979, Hughes 1988, Essink et al. 1989). Juveniles are generally able to form their own nests, or tubes, within hours—even minutes—of their release from the female marsupium (Sexton and Reid 1951, Shillaker and Moore 1987b, Barnard et al. 1991, Poore and Lowry 1997). Larger juveniles of the amphipod Leptocheirus pinguis begin building their own small tubes at the bottom of the female’s burrow (Thiel 1997a, Thiel et al. 1997). Boero and Carli (1979) also found that juveniles of the amphipod J. falcata quickly began building their tubes starting nearby, or within, parental tubes (or alongside, see Appadoo and Myers 2003). Emergent hatchlings of L. websteri fed on detritus in the maternal tube, even taking material from the mother’s gnathopods, although never from the male (Shillaker and Moore 1987b). Juveniles, however, may be evicted (Shillaker and Moore 1987b) and forced to emigrate from high adult densities, as Wilson (1989) showed in the amphipod C.  volutator. Wilson’s finding aligns with the results of Limia and Raffaelli’s investigation (1997) revealing that high densities of adult C. volutator consistently depressed the abundance of smaller conspecifics. Female C. filosa with young in the brood pouch did not construct new tubes following juvenile release (Appadoo and Myers 2003). Tube sharing is reported as being rare in tanaids, except when mancas are living in the parental tube (Larsen 2005). Tanais dulongii confines its juvenile stages to certain regions of the tube using a mucoid net (Hassack and Holdich 1987), and mancas eventually construct side tubes off the maternal tube (Bückle-Ramirez 1965). Some pseudotanaids are found, rarely, in mucus “tubes” or “nests,” which may be associated with brooding (Hassack and Holdich 1987). In the harpacticoid copepod P. wellsi, individuals of all ages, including nauplii, build tubes (Chandler and Fleeger 1984).

DEFENSE OF TUBES Male mate-guarding behavior may occur through cohabitation in tubes, as suggested recently by Conlan (2007) for Alatajassa similis (cf. by wandering and signaling in Jassa). The onset of sexual behavior in major males of the amphipod Jassa marmorata is characterized by the development of the “thumb” on gnathopod 2 propodus (a feature that is delayed until the last molt, see Conlan 1989). Borowsky (1985) noted that although younger males of J. falcata (those without “thumbed” second gnathopods) are fully fertile, they tend to remain in their own residential tubes. When outside, they will evict receptive females from the latter’s tubes and lose agonistic contests with “thumbed” males. When males molt to the terminal stage, they tend to abandon their tubes to travel to receptive females and attend them closely until they copulate. They do not evict females. Females accept the proximity of thumbed males more than they do thumbless males, and major males react



P. Geoffrey Moore and Lucas B. Eastman

agonistically toward other major males while guarding females (Prince William Sound Regional Citizens’ Advisory Council 2004). The “thumb” in Jassa functions as a label that permits females to distinguish from other individuals those males that intend to reproduce (Borowsky 1985). The behavioral ecology of hyperadult male Ericthonius and Aora spp. (see Myers and McGrath 1984, Dixon and Moore 1997 for background) awaits attention. These adaptations have been selected by increased mate competition through time, promoted by a sedentary colonial existence (Conlan 1989). In H. oerstedi, the male tears open the tube wall with its chelae in order to gain entry to the tube and thus mate with the female. When the male leaves, the female seals up the tube completely (Bückle-Ramirez 1965). In another tanaid, Leptochelia dubia, large males always won fights with smaller males, and males occupying mucous tubes or holes usually won fights against equal-sized intruders (Highsmith 1983). Similar results have been reported for aggressive encounters between tubicolous amphipods exploiting detritus around the tube mouth that can result in territorial spacing of tubes (Goodhart 1939, Connell 1963; cf. Glass and Bovbjerg 1969 on caddisfly larvae, and Chaloner and Wotton (1996) on midge larvae). The behavioral consequences of the puzzling intersexuality reported in ampeliscids (Mills 1967a) have yet to be investigated, and the parthenogenesis of C. bonnellii has not been fully explained (Moore 1981a).

TUBES AND FEEDING RESOURCES Most benthic amphipods walk like other ambulatory eumalacostracans, with the venter down and the thoracopods pushing against the substratum. Gammarids are an exception to this in slithering along sideways. Tube-dwellers, such as Cerapus and Corophium and others (when displaced), can also pull themselves along by using only the flexing action of their proximal antennal joints after the antennal spines have “grabbed” the substratum (Schram 1986). The robust antennae of Corophium can also be used as food-gathering rakes, drawing detrital particles toward the mouth of the tube, often creating a cleared star-like halo around the tube entrance when operating in deposit-feeding mode (Enequist 1949). Interactions between individuals can create a territorial spacing of tubes on a surface in some species, such as Ericthonius brasiliensis (Connell 1963). In other species, however, such as L. websteri, J. falcata, and C. bonnellii, tubes can be packed together, honeycomb-like, without agonistic interactions. Species with greater filter-feeding propensities probably tolerate the proximity of conspecifics. Togetherness of tubes also facilitates mating efficiency by limiting mate-searching time outside the tube. Aside from being merely a retreat inside which filter feeding and mating can take place in seclusion, tubes also represent surfaces for microbial colonization and growth. Tubes function as storage depots for food. If a food item is too large to be consumed all at once, it is glued to the tube and eaten later (Borowsky 1991). Barrett (1966) noted that Ampithoe valida uses its glandular pereopods to secure food to the tube. He stated that, in that species, when the animal becomes aware of a source of food outside the tube, it quickly darts out of the tube just far enough to grasp the food with its gnathopods and just as rapidly retreats back into the tube with its food. As soon as the item has been grasped, the glandular pereopods begin attaching it to the tube. As the item is being loosely attached, the mandibles are biting off small bits to be ingested. They were never observed to use the gnathopods to tear off small portions first. Holmes (1901) reported similar behavior in A.  longimana (see also Skutch 1926 on A.  rubricata). Very little is known of the lifestyle and feeding behavior of isaeid amphipods. Although the

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding group members are primarily tube-dwellers, the elongated glandular dactyls of Protomedeia and Cheirimedeia indicate a specialized tube construction function (Conlan 1983). A symbiotic feeding association has been described by Thurston et al. (1987) involving a species of Heterotanais that lives in sand-accreted tubes on the under surface of the small discoidal cheilostome bryozoan Selenaria maculata. The tanaid gains a shelter while the bryozoan colony benefits from the tanaid removing algae and detritus from the upper surface of the colony. Amphipods can also act as passive vectors for externally entangled algal spores (Buschmann and Santelices 1987, personal observation)

ECOLOGICAL ROLE OF TUBE-DWELLING CRUSTACEANS Tubicolous peracarid species, like suspension feeders in general (Wildish and Kristmanson 1997), can occur at prodigious population densities (Raitt 1937, Goodhart 1941, Sanders 1958, Casabianca 1972–73, Schäfer 1972, Hiscock and Hoare 1975, Sheader 1977, Fish and Mills 1979, Hendler and Franz 1982, Moller and Rosenberg 1982, Schaffner and Boesch 1982, Highsmith 1983, Carrasco and Arcos 1984, Oliver et al. 1984, Hassack and Holdich 1987, Franz and Tanacredi 1992, Conlan 1994, Limia and Raffaelli 1997, Havermans et al. 2007). Outer shelf habitats have been found to be dominated by tubicolous amphipods, notably surface-deposit-feeding tube-dwellers: Unciola, Ampelisca, Byblis, and Ericthonius (Boesch and Rabalais 1987). Some species may indeed be gregarious (Campbell and Meadows 1974), some invasive (Chapman and Dorman 1975, Harris and Muskó 1999). The productivity of benthic tube-dwelling amphipods (Kanneworff 1965, Klein et al. 1975, Birklund 1977, Hastings 1981, Moller and Rosenberg 1982, Dauvin 1988a,b,c, Franz and Tanacredi 1992, Sudo and Azeta 1996) is testified to by their importance on fish feeding grounds (Hunt 1925, Carrasco and Arcos 1984, Franz and Tanacredi 1992); ampeliscid amphipods even form the major part of the diet of demersal-feeding gray whales (Oliver et al. 1984, Oliver and Slattery 1985). The productivity on intertidal mud flats of the prodigiously abundant amphipod C. volutator underpins the entire food web of intertidal estuarine ecosystems throughout Europe, supporting both wading birds and fishes (Essink et al. 1989). Production-to-biomass (P:B) ratios of 6:17 were reported for this species by Moller and Rosenberg (1982). A mean P:B ratio of 10.8 was recorded by Sudo and Azeta (1996) for Byblis japonicus in a warm Japanese bay, by far the highest recorded for any ampeliscid population. The utility of P:B ratios for amphipods, however, has been called into question by Highsmith and Coyle (1991). In allopatry, black surfperch, Embiotoca jacksoni showed lower electivity for tubicolous amphipods compared to free-living gammarids (inter alia) according to Schmitt and Coyer (1983). Tanaidaceans and their mucus tubes are also easily grazed by a variety of fishes and decapod crustaceans (Modlin and Harris 1989). The presence of infaunal sand dollars may be inimical to tubicolous crustaceans (Smith 1981), but Highsmith and Coyle (1991) found that ampeliscid amphipods prey on the newly settled juveniles of the sand dollar Echinarachnius parma. The close spacing of ampeliscid tubes has also been stated to deter other suspension-feeding amphipod species from colonizing benthic habitats, as suggested by Schaffner and Boesch (1982) for Ericthonius rubricornis. Santos and Simon (1980) reported A. abdita outcompeting the polychaete Streblospio benedicti. Conversely, the presence of tube-building Tanais sp. may facilitate the recruitment of other taxa (Gallagher et al. 1983). Nest-building behavior was reduced in the amphipod A. valida exposed to pollution by no. 2 fuel oil. Recovery of nest-building activity in clean seawater was either lacking or small, indicating some damage to their nesting capability. Impairment of the chemosensory and locomotory systems may occur during exposure, which prevents amphipods from constructing nests for protection and food reserves and eventually leads animals to use their stored lipid for survival (Lee et al. 1981).



P. Geoffrey Moore and Lucas B. Eastman

The amphipods Ampithoe marcuzii and J. falcata each significantly reduced growth of epiphytes on Sargassum plants relative to amphipod-free controls, whereas E. brasiliensis had no significant effect on Sargassum or its epiphytes (Duffy 1990). The herbivorous aorid amphipod M. gryllotalpa discriminates between macroalgae for food, preferring Polysiphonia, a choice seemingly based on algal form rather than chemistry (Heckscher et al. 1996). The potential role of epiphyte mesograzers in ameliorating the risk to the host plants (of increased epiphyte drag) could be important (Duffy 1990). Interestingly, the chemical exudates from the green alga Ulva lactuca have been shown by Borowsky et al. (1987) to inhibit male responses to female pheromone in the amphipod M. gryllotalpa, an observation that highlights the need for more research on the chemical ecology of tube-dwellers. The presence of mucous tubes on seagrass blades has been shown to enhance the abundance of total meiofauna, harpacticoids, and turbellarians (Peachey and Bell 1997). By creating micro-topographic heterogeneity, tubes contribute to the structural complexity of habitats and so enhance biodiversity (Munari 2008). Tubicolous species also respond to the presence of habitat structural heterogeneity (Bros 1987). Nehring (1993) has advanced the case for considering tube-dwelling harpacticoid copepods as microbioturbators. Certainly, the biogeochemical and ecological engineering significance of tube-dwelling crustaceans is something that requires more attention (cf. Aller and Yingst 1978, Aller and Aller 2004). The flow regime around cylinders (i.e., tubes) protruding into the benthic boundary layer is complex, and stabilization versus erosion effects (note Mills 1967b, Rhoads and Boyer 1982, Statzner and Holm 1989, Nehring et  al. 1990, Friedrichs et al. 2000, Reise 2002) are markedly influenced by density of cylinders on the ground (Vogel 1988, 1994). Lynch and Harrison (1970) reported a maximum sediment accretion rate of 39 mm wk−1 caused by protruding amphipod (A. abdita) tubes (note Mills 1967b). Meadows and Tait (1989) and Meadows et al. (1990) have investigated the effects of the burrowing activities of the amphipod C.  volutator on sediment geotechnical properties (cf. Chandler and Fleeger 1984, Luckenbach 1986, Busby and Plante 2007, Bailey-Brock 2008). Interestingly, tubicolous spionid polychaetes and tanaid crustaceans co-existed with a sediment-destabilizing bivalve in laboratory experiments reported by Wilson (1984). Ampelisca amphipod tube mats may enhance the abundance of northern quahog Mercenaria mercenaria in muddy sediments (Mackenzie et al. 2006). By acting to increase surface roughness in the epibenthic water flow regime, tube-dwelling organisms generate turbulence, thereby enhancing suspension-feeding efficiency (Denny 1988).

FEEDING IN TUBICOLOUS CRUSTACEANS The treatment by Armitage et al. (1995) of feeding strategies in tubicolous chironomid midge larvae (Insecta) provides a useful comparative scheme for a consideration of feeding strategies in crustaceans. They distinguished the following feeding types:  collector-gatherers (deposit feeders), collector-filterers, scrapers, shredders, and engulfers, and piercers. Tube-dwelling crustaceans fall into four of these categories:  collector-gatherers, collector-filterers, scrapers, and shredders. Salp-associated hyperiid amphipods—adults and juveniles (Richter 1978a)—may also be carnivores, consuming salp tissue directly (Madin and Harbison 1977). By and large a tube-dwelling lifestyle does not lend itself to an obligate predatory lifestyle,, although Dixon and Moore (1997) witnessed unprompted carnivory in the ischyrocerid Ericthonius punctatus and Bousfield and Hoover (1997) speculated that Microcorophium might be a microcarnivore. Alan Myers (with Jim Lowry), however, have discovered (but not published) a predatory Grandidierella sp. from Australia, and Myers considers Bonnierella to be predatory, conjecturing that it may use its pointed epistome to pierce prey (Myers, personal communication to PGM). In general, the size of food

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding particles consumed by suspension feeders is smaller than that consumed by deposit-feeders and shredders. Miller (1984) found that Corophium ingested particles of 9 µm at a rate of more than 20 s−1. Epipsammic grazing—browsing on particles of both smaller and larger sizes than can be swallowed— has been studied in the amphipod C. volutator by Nielsen and Kofoed (1982; note also Dixon and Moore 1997 on L. websteri) who showed that it is capable of being a highly selective deposit feeder. Dixon and Moore (1997), however, found no visible evidence of a systematic rejection of particles while feeding in C. bonnellii, which would have implied some sort of sorting procedure, perhaps based on particle size or other qualities. Shallow-water tanaidaceans are usually reported as being detritivores, scavengers, or browsers (see references in Larsen 2005). Blazawicz-Paszkowycz and Ligowski (2002), studying a number of Antarctic cumacean and tanaidacean species, found that species inhabiting the shallower waters consumed almost exclusively epipelic food, although they pointed out that the food of tanaids is poorly known. Macrofaunal organisms that build tubes that project into the benthic boundary layer are usually, although not exclusively, suspension feeders (Wildish and Kristmanson 1997). These authors considered three main tube types of suspension feeders based on the ratio of height projecting above the sediment-water interface (H) and tube diameter (D): tubes normal to flow (H:D = 2–10), truncated cone tubes (H:D ≤2), and spar buoy tubes (H:D ≥20). Unsurprisingly, most of their examples related to polychaetes. However, they regarded A. abdita as a good example of the first category (see Mills 1967b). They regarded the amphipod A. valida and the tanaid T. dulongii (as T. cavolinii) as examples of species with tubes opposed to the flow. The ratio H:D, however, is inapplicable to animals with one, or both, open ends opposed to bidirectional flow. Suspension feeding may be either passive or active (see Mills 1967b). All amphipod species of the genera Byblis and Haploops are presumed to be tube-dwelling detritivores, but no direct observations of their feeding biology have been reported since the studies of Enequist (1949) on H. tubicola and Byblis gaimardi (Dickinson 1983). Haploops tubicola would be a good example of a passive suspension-feeding tubicolous crustacean (Marshall and Orr 1960). It lies slung across the mouth of its tube in an inverted hammock-like position, with its highly setose antennae protruding into the water stream passing above it to capture passing seston (Enequist 1949); feeding is initiated by turbidity of the water or currents around the tube (Mills 1967b). When A. abdita withdraws, the tube mouth shuts automatically (Mills 1967b). Filter feeding is a specialized active form of suspension feeding, one that requires (a) a filter, (b) a means of creating a current of water through it, (c) some way of actively scraping the food off, and (d) an exit for the filtered water (Marshall and Orr 1960). The strategies for capturing particles from water flowing through a tube by a range of aquatic animals have been considered by Wotton (1994). Grahame’s treatment of filter feeding in Crustacea (1983) concentrated on planktonic copepods. An earlier review by Marshall and Orr (1960) distinguished five methods of filter feeding in crustaceans, depending on which limbs bore the filtratory setae. However, their fifth category, “antennal and antennular filters,” meant to categorize Amphipoda and Decapoda, fails to encompass most of the filter-feeding Amphipoda; that is, those species that pump water through tubes and filter using gnathopodal setal baskets. Riisgård (see Chapter 15 in this volume) describes mechanisms of filter feeding in more detail. Paddles and propellers in ducts are rare in nature, but one can cite the beating (rostrocaudally flattened, leaf-like) pleopods of amphipods like Corophium as one such example (Vogel 1994, based on Foster-Smith 1978; cf. Stamhuis and Videler 1998). This attribution would characterize most of the Corophiidae (Gamble 1970a) and, indeed, the tanaid T. dulongii (= T. cavolinii; Johnson and Attramadal 1982a; note also Gamble 1970a on T. chevreuxi). The flow rate of a fluid inside any pipe is restricted by the fluid’s viscosity, which increases at low Reynolds numbers (Ward-Smith 1980). The through-tube flow produced by pleopod beating potentially serves both respiratory and feeding functions (Gamble 1970a). Harris and Muskó (1999) have investigated the former in relation



P. Geoffrey Moore and Lucas B. Eastman

to the tube-dwelling amphipod Corophium curvispinum. Research by Foster-Smith and Shillaker (1977) showed that the pumping rate of C. bonnellii was many times that of L. websteri when animals were pumping in clean glass tubes, but there was no significant difference in pumping activity when animals were allowed to establish in a detritus-lined tube within a glass tube. They discerned no sexual differences in pumping rate. Intermittent ventilation (pleopod beat rate) has been regarded as an adaptation to a tubicolous existence by Gamble (1970a). Shillaker and Moore (1987a) found that the gut contents of C.  bonnellii and L.  websteri included detritus and sand grains, together with filamentous algal remains only in L. websteri (note Drumm 2005 on two kalliapseudid tanaidaceans). The size of particles consumed by L. websteri was larger than in C. bonnellii. Riisgård (2007) has studied the pumping activity of C.  volutator in detail more recently. He showed that all the water pumped flows through the gnathopodal filter basket (which occludes the bore of the tube; see Dixon and Moore 1997 ­figure 2b) and that the pleopod pump is a low-pressure one working at between 5.1% and 11.6% efficiency. Most species of Kalliapseudidae (Tanaidacea:  Apseudomorpha) are filter feeding and thus have mouthparts and chelipeds also transformed into a filter-feeding apparatus with dense arrays of setulated setae (Larsen 2005). Dennell (1937) suggested that the tanaid Apseudes talpa also employed a secondary filter-feeding strategy, using its heavily setose maxilla and maxilliped a great deal. Larsen (2005), however, doubted that this was a “real” mode of feeding, being more a cleaning activity. Dixon and Moore (1997) distinguished two groupings within the eight species of tubicolous “corophioid” amphipods they studied: group A, which feed inside their tubes using pleopod-induced through-tube currents (C. bonnellii, L. websteri, Aora spp.), and group B, which feed outside or at the entrance to their tubes using external water currents (E. punctatus, Jassa spp.). Gammaropsis nitida exhibited traits from both groups. Ampithoid and biancolinid amphipods furnish good examples of algal shredders (Holmes 1901, Skutch 1926, Lowry 1974, Kreibohm de Paternoster 1985, Duffy and Hay 1991, Appadoo and Myers 2003). Feeding strategies of individual crustacean species tend to be flexible (Nair and Anger 1979a, Miller 1984, Shillaker and Moore 1987a) to cope with the vagaries of environmental fluctuation and seasonal availability of different food materials (Blazawicz-Paszkowycz and Ligowski 2002, Prathep et al. 2003 on tanaids; cf. also Armitage et al. 1995 on chironomids). Amphipods of the genus Corophium show considerable flexibility in feeding, with the feeding repertoire of perhaps the best researched species, C.  volutator, encompassing suspension feeding (Miller 1984, Møller and Riisgård 2006, Riisgård 2007, Riisgård and Schotge 2007), epipsammic grazing (Nielsen and Kofoed 1982, Gerdol and Hughes 1994), and deposit feeding (Meadows and Reid 1966, Miller 1984, Fenchel et al. 1975, Icely and Nott 1985, Riisgård and Schotge 2007). Corophium volutator filter feeds at high seston concentrations but switches to surface deposit feeding at low seston concentrations (Møller and Riisgård 2006, Riisgård and Schotge 2007). McLachlan (1977) has shown that tube shape and microhabitat disposition can affect feeding strategies in insect (chironomid) larvae, but equivalent work on crustaceans is lacking. Postcapture particle sorting involves the maxillipeds and maxillipedal palps (Miller 1984). The optimization of foraging strategies is presumed but reality can be complex. Stable isotope analysis has provided fresh insights into niche separation in congeneric insect (chironomid) larvae (Kelly et al. 2004), but such techniques have hardly yet been applied to tubicolous crustaceans. Suspension-feeding amphipods (Ampelisca richardsoni) in the Antarctic have been shown to have a distinctive fatty acid and stable isotope signature based on their consumption of phytoplankton cells (Nyssen et al. 2005). Sanders (1958) suggested that Ampelisca spinipes obtains its filtered food from settled detritus particles secondarily suspended by the animal’s activity. As elegantly illustrated by Highsmith (1983) and Oliver and Slattery (1985), even tanaids well known to subsist on detritus and diatoms can play a significant role as opportunistic predators (Larsen 2005). Bird and

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding Holdich (1985) associated robust mouthparts in some tanaids with a carnivorous diet (cf. fragile mouthparts being fitted for detritus feeding), but Larsen (2005) pointed out that a diet requiring mastication of diatoms or detritus requires mouthparts well developed for mastication. Gerdol and Hughes (1994), for instance, have testified to the effectiveness with which the molars of the amphipod C. volutator grind up diatom frustules. Larsen (2005) has provided a lengthy list of organisms that have been recorded as having been preyed upon by shallow-water tanaidaceans. Dixon and Moore (1997) showed that a variety of tubicolous amphipods would accept animal food (note also Enequist 1949). Bird and Holdich (1985) described the extremely filiform, tubicolous tanaid Nematotanais mirabilis from the Rockall Trough and found that its mucilaginous tubes contained numerous microorganisms they speculated might provide a food source. Bacteria are ubiquitous in aquatic environments (e.g., Muschenheim et al. 1989). Dodson (2006) stated that the tube walls of a freshwater rotifer were “impregnated” with bacteria. Crustaceans, of course, also carry epibiotic bacteria (Gillan and Dubilier 2004). Buck and Meyers (1965) isolated 87 species of bacteria from an intertidal tube-dwelling amphipod (unspecified) complex (cf. Alongi 1985). Microorganisms coat mineral grains (Meadows and Anderson 1968, Krasnow and Taghon 1997). Interestingly, however, Pelletier and Chapman (1996) found that antibiotic treatment (with penicillin-G and streptomycin sulfate) reduced variability in mortality and growth in the amphipod Corophium spinicorne. Microbes coexisting inside the tubes of the Antarctic tanaid Allotanais hirsutus are utilized for its food (Delille et  al. 1985). Kronenberger (unpublished) made some preliminary assessments of the microbiology of tubes of two marine amphipod species in Scotland. She found that the top five isolations (>95% similarity) from tubes of C. bonnellii were all γ-proteobacteria, suggesting a predominance of the orders Alteromonadales and Pseudomonadales. Unlike bacteria identified on C. bonnellii tubes, L. websteri tubes also yielded members of the α-proteobacteria. Hassack and Holdich (1987) refer to female pleopodal pumping in some tanaids transporting microorganisms into the tube, some of which then become attached to the wall. Sediment-dwelling bacteria provide the main source of food for dense colonies of tube-dwelling A. hirsutus (Hassack and Holdich 1987). More work is necessary to characterize the microbiological community and its interactions with tube-dwelling crustaceans, especially since some polychaetes are known to produce compounds that may serve to keep their inner tube surface clean (Martin et al. 2000). Williams-Howze et al. (1987), for instance, have described “microbial gardening” in the meiobenthic copepod P.  wellsi (cf. Pinn et al. 1998, Dworschak 2001 on burrowing thalassinid decapods), but little literature has been traced on small peracarids in this connection. In summer, the podocerid amphipod Dulichia rhabdoplastis grazes on diatoms that it “farms” on the detritus rods on which it lives (McCloskey 1970). Bacterial symbionts are known in the hepatopancreas of the free-living isopod Asellus (Wang et al. 2007), and commensal bacteria are known to protect shrimp embryos from fungal infection (Gil-Turnes et al. 1989), so considerable scope exists for research in this area given the confinement of tube-dwellers. Defecation in the amphipod L. websteri is followed immediately by refection (a feature especially noticeable when food is scarce). Defecation in that species was always followed by manipulation and investigation of the fecal pellet by the mouthparts. Consumption of a freshly produced pellet, however, was rare (Dixon and Moore 1997). Although C.  bonnellii—by contrast a small-particle feeder—would consume old fecal pellets (both its own and those of other species), the refection of freshly produced pellets was rarely observed (Dixon and Moore 1997). It was much less likely to recycle its fresh feces in the manner of L. websteri (Shillaker and Moore 1987a, Dixon and Moore 1997). Holmes (1901) also reported the investigation of fresh fecal pellets by another domicolous amphipod, Ampithoe longimana. The incorporation of an occupant’s fecal pellets into the walls of tubes (e.g., Johnson and Attramadal 1982a) serves to enhance the organic content of the tube wall, which is generally



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constructed from a variety of inorganic (silt, sand, foram tests, shell fragments) and organic (algal fragments, detritus) particles (see above). Microbial productivity may thereby be enhanced. In such situations (cf. Alongi 1985), colonizing microbes provide a possible alternative energy source for tube occupants, perhaps especially during times of seasonal food shortage (although it would seem unlikely that detritus is ever in short supply; if not present in suspension, then it is usually sedimented out and deposited on surfaces). The microbial content of sediments is certainly a factor determining local habitat selection by C. volutator (Meadows 1964), although it seems now (cf. Meadows 1964) that the viability of sediment microorganisms may be of little significance in habitat selection and that their role lies in their effect on the chemical and physical properties of the sediment (Deans et al. 1977). Krasnow and Taghon (1997) found that the presence of microbes tended to reduce particle selectivity in the tanaid L. dubia. To our knowledge, there is no literature on microbial “gardening” in tube-dwelling crustaceans, but this might prove a fruitful field for investigation (cf. McCloskey 1970). It is known that among some species of net-spinning caddisfly larvae in fresh waters (Hydropsychidae), abandoned nets may be reingested, recycling those animals’ investment in silk proteins (Wiggins 2004). Shillaker and Moore (1987a) noted that the marine amphipods C. bonnellii and L. websteri will reingest tube-wall material during poor feeding conditions, especially from around the tube entrances (Shillaker and Moore 1987b). Information on gut throughput times and on the filtration efficiency of crustacean tube-dwellers is scant (compared, for instance, with planktonic species). Gut residence time in C. bonnellii and L. websteri is reported to be approximately 2 h (at 13–15oC) (Shillaker and Moore 1987a). Food availability influences gut residence times (Shillaker and Moore 1987b). Defecation rates in amphipods vary with feeding conditions (Dixon and Moore 1997). In laboratory culture, defecation in J. falcata began 4–9 h after feeding (Nair and Anger 1979b), with no difference in digestion rate between males and females (cf. C. insidiosum, Nair and Anger 1979a). Assimilation efficiency in C. volutator is reportedly independent of food particle size (Nielsen and Kofoed 1982). These are all areas where more research is needed.

THE ADAPTIVE SIGNIFICANCE OF TUBE BUILDING The adaptive significance of tube building is multifarious: providing camouflage, anchorage to the substratum, enhanced filter-feeding efficiency, flexible feeding opportunity, emergency rations, and secluded mating sites. Tubes and burrows provide protection against predators, especially when they reach deep into the sediment. The scope for tube-dwellers to deliver enhanced parental care of broods of offspring in a protected milieu is well established ( Johnson and Attramadal 1982b, Hassack and Holdich 1987 on tanaids). It ranges from nest-building species (Dazai 1999) but extends also to whip-dwelling amphipods (Thiel 1997a, Thiel et al. 1997), a filter-feeding lineage represented by the podocerids, dulichiids, caprogammarids, cyamids, and caprellids (Myers and Lowry 2003). Indeed, discrete biotic microhabitats may favor the evolution of extended parental care in peracarid crustaceans (Thiel 2000). Crustaceans adopting a tubicolous lifestyle in tubes that open at both ends have also adapted morphologically by evolving an elongate habitus, smooth body, and thin cuticle. Body flexibility is a key requirement because animals (in double-ended tubes anyway) must generally be able to somersault within their tubes (Goodhart 1939, Meadows and Reid 1966, Shillaker and Moore 1987a) in order to turn round (a necessity for tube upkeep and for vigilance to be maintained, and possibly also to change feeding direction as tidal currents reverse; see Bousfield and Hoover 1997). Clearly, a heavily calcified or ornamented cuticle would impede such activity. Conlan (1983) commented that the shallowing of the coxae and flattening of Protomedeia, Cheirimedeia (Corophiidae), and Chevalia (Chevaliidae) well adapt the body to a cylindrical tube,

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding and the same could be said of all tubicolous amphipod species. Not all tubicolous crustaceans, however, inhabit tubes that open at both ends. The ampeliscid Amphipoda lie inverted, slung across the mouth of a vertical chimney-shaped tube (Enequist 1949, Christensen and Kanneworff 1965, Kanneworff 1965) in a manner reminiscent of the epifaunal amphipod Melphidippella (Enequist 1949) or an acorn barnacle. Ampeliscid amphipods have a more extensive coxal shield than many corophiids. A tubicolous lifestyle, of course, also has limitations. Foraging ability may be compromised, although this is not true of those species that drag their unattached portable (or temporarily reattachable; see Myers and Lowry 2003)  tubes around with them (quill worm-like, see Read and Clark 1999; or hermit crab-like, as in P. spinipes, see Just 1977a; or in Siphonoecetes kroyeranus, see Robertson 1888) or can swim while carrying their house (Morino 1976, Barnard et al. 1991, Lowry and Thomas 1991). Vulnerability to predators while out of tube can be countered to a degree by the adoption of nocturnal ambulation (typically by emergent males seeking mates). Mate finding remains an obvious drawback in taxa requiring copulation to achieve fertilization (as these taxa do) because most tubicolous species occupy tubes singly. In amphipods, it is the so-called “cruising male” (Borowsky 1980, 1983, Borowsky and Aitken-Ander 1991) that is nocturnally active outside tubes (DeWitt 1985, 1987, DeWitt and Levinton 1985, Shillaker and Moore 1987c, Krang and Baden 2004; note also Bird and Holdich 1989b on tanaids). Tube emergence by crustaceans and other organisms may be provoked by other biotic factors, too; for example, starvation or sensing intruder or predator presence (Meadows and Reid 1966, Fish and Mills 1979, Highsmith 1983, Dixon and Moore 1997, Kruse and Buhs 2000, Dodson 2006), as well as by abiotic factors, for example, calm (Dixon and Moore 1997) or hypoxic conditions in the surrounding water (Gamble 1970a, Harris and Muskó 1999, Meissner and Schaarschmidt 2000). Barnard et al. (1988, 1991), however, reported the tubicolous amphipod Grandidierella sp. living in foul black mud, and Gamble (1970b) showed that C. volutator, C. arenarium, and Tanais chevreuxii were all relatively resistant to anaerobic conditions. Habitat quality is clearly a determinant of distribution, but one that varies greatly between species with some being more tolerant than others. In the amphipod M. gryllotalpa, greater numbers moved greater distances when in low-quality habitats (i.e., low food availability, thin sediment layer, no crevices; DeWitt 1985). Interestingly, Meadows (1964) found that C. volutator prefers a substratum previously maintained under aerobic conditions, C. arenarium vice versa. Tube dwelling indeed may be facultative in some species, as suggested by Schaffner and Boesch (1982) for the amphipod Unciola irrorata. Marshall and Orr (1960) noted that Ampelisca gibba does not build a permanent tube. Walshe (1951) associated the presence of hemoglobin in the filter feeding tube-dwelling chironomid (insect) larvae of Tendipes plumosus with the energetic demands of turning activity after spinning the filter net (something that crustaceans do not produce, although tubicolous amphipods certainly somersault regularly inside their tubes, see above). Whether any tubicolous crustaceans carry hemolymph hemoglobin in addition to hemocyanin remains to be seen, but unpublished joint work by PGM (with P.S. Rainbow) has established the presence of hemoglobin in the leptostracan Nebalia bipes. Dispersal may then be reduced or enhanced in species with attached tubes, depending on circumstances (Munguia 2004): it will be constrained by firm attachment to solid substrata. Wilson et al. (2003) have drawn attention to the genetic isolation of populations of C. volutator, and more work needs to be done in this area (cf. also Larsen 2008 on genetic polymorphism in tanaids). However, mats of tubes can become detached by wave action during storms, and, since tubes are often attached to algae that can become detached, such material contributes to rafts of flotsam, promoting lateral dispersal (Stock and Bloklander 1952, Lowry 1974; see review by Thiel and Gutow 2005). The formation of mobile homes is an innovation in amphipods, found only within the caprellidans, of which, among the Siphonoecetini ( Just 1988), the Cerapus-group is the outstanding example (Myers and Lowry 2003). The mobile homes of Cerapus, of course, allow for deliberate



P. Geoffrey Moore and Lucas B. Eastman

relocation to and temporary fixation within better feeding areas (Myers and Lowry 2003). Such animals can even swim, by antennal beating, carrying their tubes as illustrated by Morino (1976). The facility to form attached tubes, however, allows the colonization of hard substrata in areas of strong current (a boon to small filter-feeding or detritivorous organisms capable of operating within the reduced flow regime within millimeters of the surface in even the most current-stressed situations; Lowry and Thomas 1991). A  swift current can dislodge animals outside their tubes (Borowsky 1985, Havermans et  al. 2007). Competitive advantage may depend on water movement. Thus, Nagle (1968) noted in laboratory experiments that the amphipod Microdeutopus damnoniensis was competitively superior to Corophium acutum at slack water, but the reverse was true in fast-flowing water. Foster-Smith and Shillaker (1977) found that, in the amphipod C. bonnellii, the proportion of time spent pumping was greater when animals were in moving rather than still water. Residence in tubes protects against desiccation in a species like the amphipod M. gryllotalpa that can inhabit the intertidal zone (Borowsky 1989). Johnson and Attramadal (1982a) also noted water retention in T. dulongii tubes when the intertidal zone drains. The contribution that tube-dwellers make to biofouling growths on harbor installations, ships’ hulls, and offshore constructions has been widely reported (Barnard 1958a, Onbé 1966, Poore 1968, Shyamusandari and Hanumantha Rao 1974, Hong 1983, Jianjun et al. 1989). They may also be transported around the globe by other anthropogenic agencies, for example, in ships’ ballast waters (Cohen and Carlton 1995, Carlton 1996) or during mariculture transplantation activities (Chapman and Dorman 1975). Moreover, by dint of epizoitic attachment to larger mobile mega-epibentic species, tubicolous amphipods achieve improved natural dispersal ability. Thus, a variety of tubicolous (or possibly tubicolous) amphipod species have been reported living in association with hermit crabs (Chevreux 1908, Moore 1983, Vader and Myers 1996). Those, like G.  nitida, which habitually attach their domiciles to the inside (as well as the outside) of shells occupied by hermit crabs (Vader 1971, Høberg et  al. 1982, Dixon and Moore 1997)  doubtless benefit from food particles wafted around the crab’s body during its shell-irrigation respiratory activity. Species like the amphipod Jassa pusilla also live associated with the carapaces of spider crabs and among hydroids and sponges ( Jones 1948, Moore 1981b) and may similarly benefit from food particles that escape during the crab’s foraging activities, but it is unclear whether they occupy tubes as do their cogeners. Steele et al. (1986), for instance, reported finding two “corophioid” amphipods (Ischyrocerus commensalis and Gammaropsis inaequistylis) living on the spider crab Chionoecetes opilio that apparently were not living in tubes. Such phoretic transportation benefits are not unique however: they also accrue to free-living clinging amphipods (Shoemaker 1956). The adaptations of the pleustid amphipod Myzotarsa anaxiphilius even include adhesive pads on the dactyli of the pereopods (Cadien and Martin 1999). Hamond (1967) reported that J. falcata built their muddy nests in such numbers among red algae (mostly Ceramium) off Norfolk that the algae themselves were almost invisible; an observation that PGM can confirm from Scottish waters (note also Enequist 1949 on Photis reinhardi). Nordenhaug (2004) found that form and function of the algal host was more important to amphipods than food value. In some cases, such overgrowth by amphipod tubes has been suggested as being detrimental to the host algae (Irie 1956). Stoner (1986) likewise reported the tanaids Leptochelia forresti and L. dubia as occurring nowhere in Puerto Rico as abundantly as on the tops of the calcareous green macroalgae Penicillus capitatus. Indeed, Barrios and Lemus (2000) noted that E. brasiliensis was a problem for the cultivated rhodophyte Gracilariopsis because of its massive tube-building propensities. Crustacean workers might be inspired to examine analogous possibilities to that recently described by Cairns and Wells (2008), who found contrasting modes of handling moss fragments for feeding and case building in the caddisfly Scelotrichia willcairnsi. The tubicolous amphipods M.  damnoniensis, M.  anomalus, and Corophium sextoni benefited from an association with sponges (Frith 1977). They were chemically attracted to certain sponges

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding (Frith 1976), thereby enhancing the water flow conditions of their surroundings. A similar energetically cost-effective strategy concerning crustaceans’ lack of the ability to construct their own tubes is to exploit another organism’s tube-building and pumping ability. The decapods Polyonyx (Galatheidae) and Pinnixa (Pinnotheridae) filter feed by “net casting,” in the manner of barnacles, inside the parchment tubes of the polychaete Chaetopterus (Pearse 1913), apparently to little host detriment (Grove et al. 2000). The gnathiid isopod Elaphognathia discors has recently been described as living (in female harems attended by one male) inside terebellid polychaete tubes (Tanaka and Nishi 2008). Their table 5 listed five other isopod species recorded as occupying sponge “cavities” (tube analogues). Similarly, the amphipod Colomastix pusilla lives inside the oscula of sponges (Peattie and Hoare 1981), as does the tanaid Leptochelia savignyi (Brown 1958), benefitting from sponges’ water flow thereby. Similarly, the tube tops of larger infaunal benthos, especially long-lived polychaetes (Ditrupa, Chaetopterus, Serpula, Sabella) and burrowing anemones (Cerianthus), as well as the rugose siphon tips of deep-burrowing bivalves (Mya), can be considered as Eltonian centers of action (as can hermit crabs; note Jensen and Bender 1973, Conover 1979), attracting all manner of smaller epibionts and associated flora and fauna (Daro 1970, Nalesso et al. 1995, Munguia 2004). Kanneworff and Nicolaisen (1973) reported observing Dulichia falcata females and young on fragile foraminiferan tubes attached to the free ends of the tubes of the amphipod Haploops. Resultant tube decoration, however, does not necessarily enhance tube crypsis (cf. Pardo and Amaral 2006, Berke and Woodin 2008). Such associates would benefit variously: from long-term integrity of structure held above the sediment surface, from the stronger water flow regime above the sediment boundary layer, and from the through-tube current pumped by a larger filter feeder (Foster-Smith 1978, Riisgård 1989, Forster and Graf 1995; note also Pearse 1913, Reid 1941, Statzner and Holm 1989). The possibility of enhanced tube irrigation efficiency as a result of Venturi action in elevated or exposed situations warrants attention. Reise (2002) has commented on the enhanced turbulence generated by animal constructions in sedimentary environments. Wildish and Kristmanson (1997), however, reported that no flows were induced in the tube of the amphipod Haploops fundiensis, one end of whose vertical tube is plugged with sediment. Daro (1970) reported associations between the tubicolous amphipods J. falcata and C. insidiosum with the polychaete Polydora ciliata (note also Barnard et al. 1991). The tube masses of the honeycomb worm Sabellaria number tubicolous amphipods among their associates (Wells 1970). Nalesso et al. (1995) have reported the tanaid L. savignyi as part of the tube epifauna of the polychaete Phyllochaetopterus socialis (cf. Pearse 1913, Lewis 1998). Tube-dwelling Corophium spp. and L.  savignyi have also been encountered living inside burrows excavated in wood by the isopod Limnoria tripunctata (Sleeter and Coull 1973). Moore and Cameron (1999) described finding a “furry collar” of tubes of the amphipod Photis longicaudata clustered around the tube tops of the burrowing anemone Cerianthus lloydii, with the amphipods presumably gaining proximity protection from the anemone in addition to the benefits already stated. Aquarists know that burrowing anemones like Cerianthus pack quite a sting (Fenner 2008). Crustacean resistance to cytolytic sea anemone toxins has been investigated (Giese et al. 1996), but no data are available for amphipods. Another tubicolous amphipod, E. rubricornis, was the dominant associate of a large dead antipatharian coral colony sampled at 106 m off California (Love et al. 2007), doubtless thereby gaining useful elevation into the water column. A more effective and efficient use of habitat space and colonizing ability generates competitive advantage for tubicolous species, at least in the early stages of succession (Poore 1968, Jacobi and Langevin 1996). Closely coexisting tubicolous species may partition space in relation to different microhabitat requirements (Shillaker 1977, Hughes 1978). The cryptic shelter offered by tubes is clearly no obstacle to predation by megafauna that can either sift through surface sediment (wading birds) or consume sediment wholesale (gray whales). In addition, smaller predators like nemertine worms (Kruse and Buhs 2000) have morphologies



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well adapted to poking down the bore of tubes; some polychaetes do too (note Redmond and Scott 1989). However, the narrower bore tubes of peracarids (cf. tubicolous polychaetes) might offer more protection from foraging nemertines (Roe 1976). The development of strong chelate gnathopods in tanaids and certain amphipods doubtless serves to offer any such interloper a timely rebuke (Highsmith 1983). Organisms like some “corophioid” amphipods that lack such defensive structures (one pair of gnathopods being adapted to filter feeding) are likely to fall prey to predators with probing proboscis (nereids) or chelate appendages (crangonid shrimps). Errant males, in particular, are more vulnerable to predation, be they amphipods (Nelson 1979) or tanaids (Mendoza 1982, Highsmith 1983). The sexual dimorphism of gnathopod form in the tubicolous amphipod L. websteri did not appear to influence the process of food capture, but it was reflected in how the gnathopods were used subsequently in grooming and food handling (Dixon and Moore 1997). Whip-dwelling dulichiid amphipods may achieve reduced exposure to epibenthic predators by virtue of their elevation above the viscous benthic boundary layer (Thiel 1997b, but note Thiel 1998). Tubes represent considerable energy investment, and most of the activity of tubicolous species, including reproduction, occurs inside them (Borowsky 1991). They enhance individual survivorship (Nelson 1979, Cuker et al. 1992), so it is advantageous for animals to conduct as many activities inside them as possible (Hassack and Holdich 1987, Borowsky 1989). They can allow for colonization of otherwise objectionable habitats (Gamble 1970b). “Diogenes syndrome” (an undue slur on the reclusive character of the cynic Diogenes of Sinope?) is a behavioral disorder in humans characterized by extreme self-neglect. Crustaceans, the hermit crab Diogenes included, care more for their “homes without hands” than that.

FUTURE DIRECTIONS The crustacean tube-dwelling lifestyle has historically received little attention, with many researchers ignoring crustaceans in discussions of tube-dwelling marine species. The work that has been done has mostly focused on shallow-water species because of comparative ease of study, whereas deep-sea tube-dwelling species are poorly studied and must receive attention now that researchers have access to technologies that facilitate deep-sea research. Amphipods have been the subject of the bulk of crustacean tube-dweller research, while other groups (such as copepods, decapods, and tanaids) lack detailed descriptions. The effects of parasites and epibionts on tube-dwellers’ feeding are also poorly studied.

CONCLUSIONS Tube-dwelling is a lifestyle present across crustacean taxa such as Copepoda Harpacticoidea, Peracarida (Amphipoda, Isopoda, Tanaidacea), and Decapoda. Crustacean tubes can be made out of silt and sand grains, foraminiferan tests, algal fragments, echinoid spines, and other detritus, and are typically cemented and lined with silk. Some species occupy tubes made by mollusks or worms. The body shape of these crustaceans is usually elongate and cylindrical to help them move more efficiently within tubes. Many species share tubes with scaleworms or other crustaceans and can be vulnerable to infestations and parasites. Due to the importance of tubes for mating, feeding (generally of the filtering type), microbial colonization, growth, and food storage depots, they are often defended from intrusion. Tube-dwelling crustaceans play an important ecological role: because they can occur in massive numbers, they serve as an important part of diets of fish and birds around the world. They can also increase biodiversity by introducing heterogeneity into marine topography. Tube-dwelling

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The Tube-dwelling Lifestyle in Crustaceans and Its Relation to Feeding crustaceans employ a variety of different feeding styles and can be grouped into collector-gatherers (deposit feeders), collector-filterers, scrapers, shredders, engulfers, and piercers. The tube provides adaptive benefits to the crustacean by providing camouflage, anchorage to the substratum, enhanced filter-feeding efficiency, flexible feeding opportunity, emergency rations, and secluded mating sites.

ACKNOWLEDGMENTS PGM is grateful to John Fleeger (Louisiana) and Graham Bird (New Zealand) for helpful comments related to tube-building harpacticoid copepods and tanaids, respectively. Paul Clark (Natural History Museum, London) kindly arranged for the photocopying of some key material. Peter Meadows (Glasgow) helped with geotechnical references. Alan Myers (Cork) kindly suggested improvements to an earlier draft. Jim Atkinson’s (Millport) ever-helpful comments, particularly in areas of overlapping remit, have been most appreciated.

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4 BURROW DWELLING IN CRUSTACEA

R. James A. Atkinson and Lucas B. Eastman

Abstract Burrow-dwelling crustaceans are widespread across many groups, most notably the Stomatopoda, Isopoda, Amphipoda, Caridea, Astacidea, Anomura, Thalassinidea, and the Brachyura, with the last two groups being the best studied. Crustacean burrows are structurally diverse. There is an extensive record of fossil burrows, many of which are attributable to crustaceans, demonstrating that their burrowing lifestyle is ancient and varied. The methods used in burrow construction and maintenance vary across the crustacean groups, and many show morphological and physiological adaptations to their burrowing mode of life. A burrow not only provides a crustacean with a refuge from predators but also has other functions, serving as protection from environmental extremes, and providing a locus for feeding, territorial, and reproductive activities. Crustacean burrowers are important ecosystem engineers, disturbing sediment, changing bed topography, and modifying the flux of oxygen and nutrients, with positive and negative ecosystem effects. Interspecific associations are common in burrow-dwelling crustaceans.

INTRODUCTION The burrow-dwelling lifestyle is widespread among marine, freshwater, and terrestrial taxa and is characteristic of many crustaceans. The best-known fossorial examples among crustaceans are found in decapods, particularly semiterrestrial crabs (e.g., Vannini 1980) and littoral and shallow sublittoral thalassinidean mud shrimps (e.g., Dworschak 1983, Atkinson and Taylor 2005). There is much more information on these than other groups, reflecting both trends in researcher interest and ease of observation. As a result, these receive more attention than other groups in this chapter. There is also extensive geological interest because burrows are common trace fossils, and many of these are attributable to crustaceans.

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Many crustaceans are obligate burrow builders; others are facultative burrowers. They show a range of adaptations to their burrow-dwelling mode of life. Burrows may normally be occupied by an individual, a reproductive pair (Karplus 1987), a family group (Linsenmair 2007), or a colony (Atkinson et al. 1982). In the case of the caridean shrimps Alpheus inca and Alpheopsis chilensis, a quartet comprising a reproductive pair of both species co-occupies a burrow (Boltaña and Thiel 2001). Burrow-dwelling crustaceans have many burrow associates, and, conversely, many crustaceans co-occupy the burrows of other species. Burrows have several functions, including a refuge from predators and adverse environmental conditions, and they may serve as a locus for feeding and reproductive activity. Some species spend all of their adult lives in their burrows; others emerge periodically to engage in reproductive, feeding, and other activities. Crustacean burrow-dwellers can profoundly affect the environment where they occur, having both positive and negative environmental effects. Terminology The term “burrowing” is legitimately used in relation to animals that bury in the sediment for concealment, to describe movement through sediment without forming burrows, and to describe the behavior of animals that create burrows. Some crustaceans, for example, the anomuran mole crabs Emerita spp. and the brachyuran masked crab Corystes cassivelaunus, bury in the sediment by a process known as back-burrowing (Trueman 1970, Warner 1977): no burrow is produced (Faulkes 2013). Various amphipods, for example, Haustorius arenarius, leave distinct traces as they move through sediment, but again no burrow is formed ( Jensen and Atkinson 2001). Traces formed by the passage of animals through sediment were termed intrastratal trails by Frey (1973). The physiological challenges of burying as opposed to burrow dwelling have been examined by Atkinson and Taylor (1988, 1991) and Taylor and Atkinson (1991). This chapter deals only with those crustaceans that occupy burrows. Ichnologists who study animal traces for paleontological purposes have carefully (but not unanimously) defined burrowing and burrows. This account mostly follows the approach taken by Frey (1973) and Bromley (1996) in defining burrows, burrowing, and burrow components. Thus, according to Frey (1973), a burrow is a bioturbation structure as distinct from a boring, which is a bioerosion structure. However, as shall be seen, this distinction may not be clear-cut, and many researchers, even among ichnologists, refer to borings sensu Frey as burrows. Burrows may be simple or complex; in the latter case, they are referred to as burrow systems by Frey (1973). However, the term “burrow system” may also be used to describe the whole burrow in contrast to parts of it. For example, researchers using underwater television to count the burrows of Nephrops norvegicus for stock assessment purposes may refer to a configuration of burrow openings that are judged to be interconnected as a burrow system (ICES 2007, Morello et al. 2007). Following Frey (1973), vertical or predominantly vertical burrow components are referred to as shafts, and horizontal or predominantly horizontal components as tunnels or galleries, although the latter term has also often been applied to dilations within burrows, an approach favored by the present authors. Frey (1973) regarded a burrow as an excavation within unconsolidated sediment. However, burrows may be produced in several ways. Excavation as defined by Bromley (1996) is “a burrowing technique that involves loosening of compacted substrate and transporting it . . . so as to create an open space.” This appears to be the most common burrow creation method among crustaceans, moving sediment from one location to another either within the burrow or to the sediment surface. Burrows may also be produced by compaction of the sediment as a result of passage of an animal through it, termed compressional burrowing by Bromley (1996), a common method in vermiform species. Recent work has shown that crack propagation is implicated as animals move through muddy sediments, and a burrow may be the result (Dorgan et al. 2006). The method of burrowing

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Burrow Dwelling in Crustacea and the type of burrow produced reflect the burrower’s body plan and its digging tools (Trueman 1975, Bromley 1996). The articulated limbs of crustaceans provide them with the means to be effective burrow constructors, although the method employed varies across crustacean groups as will be seen. Burrow structure also reflects lifestyle: there have been various attempts to classify burrows on this basis. This aspect is explored in the subsequent section on burrow function. Descriptive classification schemes are for cataloging convenience:  often, the boundaries between categories are blurred. Thus, there are firmground burrowers that are similar in many respects to hardground borers. Also, some hardground borers line their borings with particulate sediment. Burrowers in loose sediments such as sands line their burrows to consolidate the walls and prevent collapse. In this case, the burrow has features in common with a tube (see Chapter 3 in this volume). Also, some burrowers extend their burrows with constructions at their openings, these being analogous to tubes in some cases. The literature is not consistent on terminological matters: some structures referred to as burrows are technically tubes, some are borings, but the lifestyle implications are usually similar. There is also the special case of hermit crabs that may be considered to be carrying a structure (usually a gastropod shell) in some ways analogous to a burrow (see Chapter 6 in this volume). Finally, the authors prefer to use the term “opening” for a burrow aperture rather than the word “entrance.” Although it is perfectly legitimate for a structure to have an entrance, the term could also be taken to imply the entrance behavior of the occupant, which might be inappropriate for a given burrow opening.

BURROW-DWELLING CRUSTACEA Meiofaunal Crustaceans Meiofauna may move through the interstices of coarse-grained sediment with little disturbance of the grains, but in finer-grained or poorly sorted sediments disturbance inevitably occurs (Reichelt 1991). As they move through such sediment by means of what has been termed intrusion burrowing (Bromley 1996), the meiofauna displace the grains and can have profound effects on the sediment, essentially homogenizing it. Biogenic effects by small macrofauna and meiofauna can be subtle, blurring sediment structures (physical and biogenic) without completely obliterating them. The term cryptobioturbation has been used to describe this effect (Howard and Frey [1975] initially used this term to describe the effects of amphipod activity in sediment), easily overlooked evidence that sediment has been biogenically reworked at a small scale (Pemberton et al. 2008). However, some meiofauna such as harpacticoids form minute, usually short-lived mucus-lined structures within the sediment (Chandler and Fleeger 1984). Little is known of biogenic structures at this scale (Reichelt 1991). Mucus-lined microburrows and microtubes may be widespread. Stomatopoda Many species of stomatopod within the superfamilies Bathysquilloidea, Squilloidea, and Lysiosquilloidea occupy burrows in sediments, although not all within these groups are burrow-dwellers (Reaka and Manning 1987). Although there are many general statements about their burrow-dwelling lifestyle, there have been few detailed studies of their burrows (e.g., Myers 1979, Hamano et al. 1994, Atkinson et al. 1997). The Gonodactyloidea also contains burrowing species, but many species do not burrow but rather occupy holes and crevices in hard substrata, often those created by other species (Reaka and Manning 1981, 1987). These refuges may be modified by



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B

A

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F E

Fig. 4.1. Burrows of Stomatopoda, Isopoda, Amphipoda, and Caridea. (A) The stomatopod Squilla mantis, from resin cast of burrow illustrated in Atkinson et al. (1997). (B) The isopod Natatolana borealis within its burrow; note the lighter-toned sediment adjacent to the burrow wall and the patches of anoxic sediment away from the burrow lumen. Photo by R.J.A. Atkinson. (C) The amphipod Trinorchestia sp. (either T. trinitatus or T. longiramus) from photograph of plaster (gypsum) cast of burrow in Ohshima (1967; as Talorchestia brito). (D) The caridean Alpheus floridanus, from photograph of resin cast of burrow in Dworschak and Ott (1993). (E) The caridean Alpheus bellulus, from photograph of resin cast of burrow illustrated in Yangisawa (1984). (F) The caridean Alpheus djiboutensis, redrawn from illustration in Karplus et al. (1974), this based on a resin cast of the burrow but with adhering debris removed. Scale bars: A, D, E, F = 10 cm, B = 1 cm, C = 5 cm.

the gonodactyloid occupants and are defended vigorously (Reaka and Manning 1981). The high levels of aggression that gonodactyloids exhibit toward conspecifics and intruders have been attributed to the shelter resource being in short supply. In contrast, the squilloid stomatopods that construct burrows in particulate sediments are less aggressive. Sediment is not a limiting resource: burrows are defended but, if necessary, new ones can be constructed (Caldwell and Dingle 1975, Dingle and Caldwell 1978). Dingle and Caldwell (1978) also noted that those squilloid species that construct simple burrows are less aggressive than those that construct more complex ones. Stomatopod burrows are of relatively simple structure, and most of those described consist of a horizontally extended U-shaped burrow (Fig. 4.1A). One surface opening is usually larger than the other, and the tunnel may have a mid-point constriction (Hamano et al. 1994, Atkinson et al. 1997). Where branch tunnels are present, these appear to relate to burrow deepening (Myers 1979, Atkinson et al. 1997). In some species, the burrow may be several meters deep and vary in structure seasonally (Myers 1979). Isopoda Isopod crustaceans are a common component of marine sandy beaches (Dahl 1952–1953), but most of these do not form burrows. Tylos granulatus is an example that constructs a simple vertical burrow in beach sand from which it emerges at night (Ohshima 1967). Morphological adaptations to burrowing through sand have received detailed attention (e.g., Griffith and Telford 1985), but burrow-forming techniques are less well known. Much more is known about isopods such as Limnoria spp. that bore into hard substrata such as timber (Cragg et al. 1999) or tubicolous isopods (see Chapter 3 in this volume) than about species that burrow into sediment. Some isopods can

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Burrow Dwelling in Crustacea both bore into hard materials and burrow into sediment. An example is the Australasian isopod Sphaeroma quoianum that has invaded North America (Davidson 2008, Davidson et  al. 2008a, 2008b). It can penetrate sedimentary rock, wood, and estuarine banks where its numerous anastomosing burrows may cause bank erosion (Talley et al. 2001, Davidson 2008). Sphaeroma species are well-known borers, and the plasticity of excavatory behavior seen in S. quoianum is likely to be a feature of other species within the genus. The isopod Paragnathia formica is an interesting example that occupies burrows in saltmarsh banks. A male creates a burrow that is co-occupied by a harem of females. When the females are gravid, the burrow is permitted to be flooded and larvae swim out to become ectoparasitic on fish; after feeding, they return to the estuarine banks in which they burrow and molt into the next larval stage (there are three), and the cycle is repeated. Last, the early settling final stages become females, entering male burrows, and the later settlers become a new generation of males (Tinsley and Reilly 2002). Another burrow-forming example is the scavenging isopod Natatolana borealis. This species gorges itself on carrion and then burrows into the sediment. Taylor and Moore (1995) showed that when it did so in mud, then simple U-shaped burrows were formed (Fig. 4.1B). Isopods are successful colonizers of terrestrial environments (Little 1983). Many terrestrial species dig through soil and leaf litter (without making burrows) or occupy interstices beneath stones, fallen branches, and the like (Oliver and Meechan 1993). Burrow-dwelling, however, is sparsely reported. An interesting example is the burrow-forming, desert-dwelling Hemilepistus reaumuri. In this social species, family groups occupy burrows with a single opening:  these are defended by family members (Linsenmair 1984). A fully developed inclined burrow descends to a depth of from 40 cm to 1 m, is dilated at the base, and has side branches occupied by the juveniles (Shachak et al. 1979, Linsenmair 2007). Given the severe environment, the burrow is essential for survival, and the foraging parent isopods show remarkable homing behavior (Hoffmann 1984). The homing behavior of these isopods is essential not only for bringing food to their offspring, but also because the clay soil in which the burrows are established in spring (Coenen-Stass 1984) is impenetrable in the summer, preventing new burrow formation (Linsenmair 1984, 2007). Some Porcellio species are reported to construct burrows in sandy sediments (Linsenmair 1984, 2007). Although less permanent than the burrows of H. reaumuri, they, too, are related to reproductive behavior, and Porcellio species return to them after foraging excursions (Linsenmair 1984, 2007). It is likely that more oniscoids create burrows than the literature currently reflects. Amphipoda As with Isopoda, information on burrow-dwelling Amphipoda is relatively sparse. This is in contrast to an extensive literature on tube-dwelling amphipods (see Chapter 3 in this volume) and of those that move through sediment without forming burrows (Bousfield 1970). Corophium volutator is one of the best-known examples of a burrow-building amphipod, typically occurring in muddy sediments (Häntzschel 1939, Green 1968, Schäfer 1972). Both it and the closely related Corophium arenarium that inhabits sandier sediments (Ingle 1966)  construct U-shaped burrows, typically in estuarine shores. Talitrid amphipods reside high on sandy beaches (Dahl 1952–1953): they burrow into the sand, which is often extensively “peppered” with the holes that are formed by this activity, to form simple, vertical shafts (Fig. 4.1C; Ohshima 1967, Dashtgard and Gingras 2005). These amphipods usually emerge at night to forage over the shore and are able to orientate using celestial and landmark cues (Bregazzi and Naylor 1972, Hartwick 1976). Their burrows, however, are not permanent structures (Dahl 1952–1953), and burrow depth appears to be determined by sand moisture content (Williams 1983).



R. James A. Atkinson and Lucas B. Eastman

Leptocheirus pinguis and Casco bigelowi are examples of shallow subtidal burrow-dwelling amphipods: young are liberated within parental burrows constructed in muddy sediment by female amphipods (Thiel 1999). These burrows are of simple structure but are deep enough to protect the inhabitants from predation. Another example of a subtidal burrow-dwelling species is the relatively large, deposit-feeding Maera loveni whose burrowing behavior was described by Atkinson et  al. (1982). The species creates complex burrows in muddy sediment, with interconnected components created by many individuals, a rare example of colonial burrowing in amphipods. Caridea Burrow-dwelling is a common lifestyle amongst the Alpheidae (Banner and Banner 1966). Alpheids are associated with many burrow-dwelling species (see summary in Dworschak and Coelho 1999). In these associations, the shrimp may be the burrow constructor or may occupy the burrow of another species. Burrow-building alpheids that live in symbiotic association with gobiid fish are the best known and may be facultative or obligate (Karplus 1987). Not all alpheid burrow-dwellers are symbionts. For example, individual Alpheus glaber and A. migrans construct independent burrows in sublittoral muddy sediments (Dworschak and Pervesler 2002, Atkinson et  al. 2003). In some species, reproductive pairs of shrimp occupy burrows in littoral sediments (Schein 1975, Basan and Frey 1977, Dworschak and Ott 1993, Mathews 2002). Alpheid burrows are generally shallow constructions that range from simple U-shaped burrows to complexly branched structures with numerous openings (Schein 1975, Basan and Frey 1977, Dworschak and Ott 1993, Mathews 2002; see also Farrow 1971, Yanagisawa 1984). Burrow openings and tunnel sections may be elaborated with embedded shell and coral fragments, giving reinforcement and preventing sediment sliding into burrow openings (Farrow 1971, Karplus et al. 1974). Burrow structure can vary with the grade of substratum (Palomar et al. 2005). When burrowing in coarse deposits, deviations around buried stones and shells further add to burrow complexity (Farrow 1971, Karplus 1987). Alpheid burrows are illustrated in Fig. 4.1D–F. Shrimps from other families also occupy burrows, but information is sparse. Records are usually for those living in the burrows of other species (see the section “Associations”), but some appear capable of independent burrow construction, for example, the processid Processa edulis (see Thompson 1856). Astacidea Detailed descriptions of burrows and burrowing behavior exist for freshwater crayfish and nephropid lobsters, particularly the Norway lobster N. norvegicus, an important commercial species that burrows in muddy deposits in northeastern Atlantic coastal waters and in the Mediterranean Sea. In the case of N. norvegicus, the research impetus has been the need for accurate burrow identification during stock assessment surveys based on enumeration of burrows observed in underwater television surveys (Marrs et al. 1996, Smith et al. 2003, Bell et al. 2006, Morello et al. 2007, ICES 2007, 2008). The burrows of N.  norvegicus (Fig. 4.2A,B) vary from simple horizontal tunnels with two surface openings to complexly branched systems with numerous openings (Marrs et al. 1996). Still-camera burrow surveys are used for stock assessment of Metanephrops challengeri in New Zealand waters, a species whose burrows are similar to those of N. norvegicus (ICES 2007). Other Metanephrops species occupy burrows, as do Nephropsis species, but little is known about these animals. Nephropid lobsters of the genus Homarus readily construct burrows when they are juveniles and may do so subsequently (Cobb 1971, Dybern 1973, Berrill 1974, Cooper and Uzmann 1980,

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A

C

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Fig. 4.2. Astacidean burrows. (A) Nephrops norvegicus, plan view of burrow of adult with adjoined burrow of juvenile, from photograph of resin cast of burrow in Marrs et al. (1996). (B) Nephrops norvegicus at its main burrow opening, field photo by R.J.A. Atkinson. (C) Parastacus defossus from resin cast of burrow illustrated in Noro and Buckup (2010; number of functional openings unclear). (D) Engaeus tuberculatus communal burrow complex, redrawn from diagrammatic illustration in Horwitz et al. (1985; horizontal line denotes water table). Scale bars: A, D = 10 cm; B, burrow opening width ca. 8 cm; C = 40 cm.

Botero and Atema 1982), although occupying crevices in rocky substrata or inhabiting a range of other shelters is more common for adults (Childress and Jury 2006). Deep-water adult H. americanus occupy burrows (Cobb and Castro 2006): those on open muddy grounds may occupy burrows or excavate depressions (Cooper and Uzmann 1980). Although burrow-dwelling in adult H. gammarus is known (Dybern 1973), it appears to be less common than in H. americanus. Many species of freshwater crayfish, including semiterrestrial species, are habitual burrow-dwellers (Fig. 4.2C,D), and a capability for burrowing appears to be widespread (Berrill and Chenoweth 1982). American burrow-dwelling crayfish have been divided into those that rarely leave their complex and individually occupied burrows, those that emerge to forage when their habitat is seasonally inundated, and those that burrow only at certain times, for example, during droughts, in the winter, or when ovigerous (Hobbs 1942). Many Australian species are burrow-dwellers, and these, too, have been classified depending on whether they are in or connected to a permanent water body, connected to the water table, or independent of the water table: the last of these categories contains species that do not fit Hobb’s scheme (Horwitz and Richardson 1986). Other burrow-related classification schemes are those of Riek (1972) for parastacids and Hasiotis and Mitchell (1993) for fossil burrows, based on varying complexity. Some crayfish excavate burrows several meters deep (Grow and Merchant 1980, Hobbs and Rewolinski 1985, Richardson 2007). In



R. James A. Atkinson and Lucas B. Eastman

many species, each burrow is occupied by a single individual; others live as pairs or in communal burrows that may be of a complex structure (Fig. 4.2D), including the attached burrows of juveniles (Williams et al. 1974, Horwitz et al. 1985, Noro and Buckup 2010). Excavated sediment may form distinctive chimneys around burrow openings, and these may be plugged during dry weather (Williams et al. 1974). In some cases, it is evident that chimneys are constructed to prevent inundation (Suter and Richardson 1977); they have also been attributed to the maintenance of high burrow humidity in the dry season (Noro and Buckup 2010). Burrow architecture of a given species may vary depending on factors such as environmental conditions and the number of individuals in occupancy (Hobbs 1981, Horwitz and Richardson 1986, Gherardi 2002). Many authors, including those listed earlier, have given generalized descriptions of burrow morphology, and a few (e.g., Hasiotis and Mitchell 1993, Noro and Buckup 2010) have used casting materials to reveal the fine details of burrow structure. Most semiterrestrial crayfish rarely leave their burrows, but Richardson (2007) points out that Euastacus sulcatus is an exception that makes extensive foraging excursions. Principally aquatic crayfish may also make extensive terrestrial movements, probably related to changing hydrological conditions (Wygoda 1981). Anomura There is a paucity of information on burrow-occupancy in anomurans. Birgus latro (Coenobitidae), the large land-dwelling robber or coconut crab, is able to construct a burrow, although it will also find shelter in other locations such as rock crevices, hollow logs, and among roots (Held 1963, Cameron 1981, Fletcher 1988, Hartnoll 1988, Wolcott 1988, Greenaway 2001). Coenobita spp. may also create burrows, although, like B. latro, they make use of a variety of other retreats, including burial in damp sand (Vannini 1975a, 1975b, Wolcott 1988). Other relevant literature includes brief references to species of squat lobsters, for example, Munida rugosa (Galatheidae), observed within the burrows of other species (Atkinson et al. 1977), or galatheids such as M. tenuimana associated with burrows in underwater photographs (Hartnoll et al. 1992). Whether or not some of these galatheids are able to construct their own burrows is unclear. Thalassinidea In contrast to the Anomura (a group that at one time contained the Thalassinidea), there is an extensive literature on burrows and burrowing behavior in thalassinidean mud shrimps. The infraorder Thalassinidea has recently been divided into two intraorders, the Axiidea and Gebiidea (De Grave et al. 2009, Robles et al. 2009), but, because of familiarity, Thalassinidea and the derivative term thalassinidean are retained in this chapter. Although bearing the designation mud shrimps, this group includes species that burrow in a wide range of particulate sediments and also firmground burrowers and borers in solid substrata. The group has recently experienced a resurgence of scientific interest, with much of it focused on the environmental impact of these burrowing crustaceans that are often found at high population densities. Their burrows exhibit a wide range of structure (Figs. 4.3 and 4.4), reflecting their differing morphologies and lifestyles, and ranging from simple U-shaped burrows to complexly branched structures. The burrows of Upogebiidae and Callianassidae are more studied than those of members of other families. This reflects both their abundance and that upogebiids and callianassids have many littoral representatives so that their burrows are accessible to study. Some occur at astonishing density, exceeding 1,000 individuals per m2 in the case of Nihonotrypaea harmandi on Japanese tidal flats (Tamaki et al. 1997).

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Fig. 4.3. Line drawings of thalassinidean burrows (side views). (A) Upogebia pusilla, from resin cast of burrow illustrated in Dworschak (1983). (B) Nihonotrypaea petalura, from resin cast of burrow illustrated in Shimoda and Tamaki (2004). (C) Paratrypaea bouvieri, from resin cast of burrow illustrated in Dworschak and Pervesler (1988; as Callianassa bouvieri). (D) Glypturus acanthochirus, from resin cast of burrow illustrated in Dworschak and Ott (1993). (E) Pestarella tyrrhena, from resin cast of burrow illustrated in Dworschak (2001; as Callianassa tyrrhena). Scale bars: A, D, E = 10 cm; B = 5 cm; C = 1 cm.

Relatively simple U-shaped burrows are seen in upogebiids (Dworschak 1983) (Fig. 4.3A). These burrows may be elaborated in a number of ways. Dilations are often present in which the occupant is able to turn by somersaulting, and the pattern of such dilations and other burrow features may be species-specific rather than responses to differing environmental conditions (Atkinson et  al. 1998, Kinoshita and Itani 2005). There may be more than one U-shaped section (Dworschak 1983, Nickell and Atkinson 1995), and there may be horizontal and vertical branch tunnels (Astall et al. 1997, Hall-Spencer and Atkinson 1999). A vertical or oblique descending shaft, from the base of the U-section, is quite common: this may be branched or unbranched (Kinoshita and Itani 2005). In the burrows of Upogebia major and U. yokoyai, this shaft may descend for more than a meter, and, in the case of U. major, the total burrow depth may be around 2.5 m (Kinoshita 2002, Kinoshita et al. 2010). Callianassid burrows show great variation in complexity and often penetrate deeply into the sediment (Fig. 4.3B–E). Most are multibranched and have two or more surface openings (e.g., Dworschak and Pervesler 1988, Griffis and Suchanek 1991, Dworschak 2001, 2002, Dworschak et al. 2006), although single-opening burrows are reported (Fig. 4.3B) that are not an artifact of incomplete resin-casting of the burrow (Shimoda and Tamaki 2004). Complex morphologies are seen in deposit-feeding species in which lattices of interconnecting tunnels are developed at particular depth horizons (e.g., Fig. 4.3C). Many callianassids accumulate seagrass or other vegetative material in burrow galleries constructed for this purpose (Fig. 4.3D,E), but with considerable interspecific

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Fig. 4.4. Photographs of thalassinidean burrows. (A)  Axius stirhynchus within its burrow, aquarium photograph by R.J.A. Atkinson. (B) Numerous burrow openings of Calocaris macandreae and Nephrops norvegicus (N). Field photograph courtesy of M. Service. Scale bar: A = 1 cm; B, Calocaris burrow openings ca. 2 cm (oblique camera view).

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Burrow Dwelling in Crustacea variation (Griffis and Suchanek 1991, Dworschak 2001, Dworschak et al. 2006, Kneer et al. 2008). For a given species, burrow complexity may vary in response to prevailing conditions, as has been shown for Callianassa subterranea and Biffarius (as Callianassa) filholi (Nickell and Atkinson 1995, Rowden and Jones 1995, Stamhuis et al. 1997, Berkenbusch and Rowden 2000). For other thalassinidean families, there is less information on burrow structure. Examples include the laomediid Jaxea nocturna that constructs deep, branched burrows, often exhibiting a loose spiral structure and with several openings to the surface, some of which are characteristically plugged so that at least two remain functional at any given time (Pervesler and Dworschak 1985, Nickell and Atkinson 1995). Neaxius acanthus (Strahlaxidae) constructs burrows in carbonate sands in seagrass meadows (Farrow 1971, Kneer et al. 2008, Vonk et al. 2008). The inclined burrow has a single opening and dilated subsurface chambers (in which seagrass is accumulated) penetrating to a depth of around 50 cm. A simple U-shaped burrow constructed in the laboratory by the little-known axiid Axius stirhynchus is shown in Fig. 4.4A: field burrows are probably more complex. The calocaridid Calocaris macandreae (emerging evidence suggests that this family will be subsumed within Axiidae; Robles et  al. 2009)  constructs complex branched burrows characterized by tripartite burrow junctions, semicircular galleries, and numerous openings (Figs. 4.4B and 4.5A). Unlike most thalassinideans, the burrow is relatively superficial, and the main development is in the horizontal plane (Nash et al. 1984). Principally a deposit-feeder, “microbial gardening” has been suggested from the burrow structure (Nash et al. 1984), and, unusually for a thalassinidean, C. macandreae is capable of carnivory and will also cache animal material within its burrow (Pinn and Atkinson 2010). The deepest burrow of a sublittoral crustacean appears to be that of the axiid thalassinidean Axius serratus that may penetrate muddy sediment to depths in excess of 3 m (Pemberton et  al. 1976). The mounds around the burrow openings of mud lobsters (Thalassinidae) of the genus Thalassina (see Davie 2002), of which the best known is T.  anomala, are probably the largest structures constructed by a crustacean, being 3 m high in some cases with a basal area that can exceed 36 m2 (Verwey 1930, Macintosh 1988, Tan 2001; Fig. 4.5B). The most complex crustacean burrows are those reported by Dworschak and Rodrigues (1997) for the axianassid Axianassa australis. The multibranched burrow has numerous corkscrew-like spiral shafts interconnected with horizontal galleries (Fig. 4.5C) and extends to more than a meter in depth (Dworschak and Rodrigues 1997). Brachyura Burrow-dwelling crabs are found in marine, estuarine, and freshwater environments, and the best known examples are semiterrestrial and terrestrial species. There are fewer detailed examples of burrow-dwellers among species that are fully aquatic. Crabs demonstrate a range of adaptations to terrestrial life, and many of them construct burrows: some are dependent on frequent access to permanent water bodies, others are not, and there is some debate about appropriate terminology. Several classification schemes have been proposed for what have been termed “land crabs,” and terminological problems have been discussed extensively (Bliss 1968, Warner 1977, Powers and Bliss 1983, Rebach and Dunham 1983, Atkinson and Taylor 1988, Burggren and McMahon 1988). Although not confined to the following groups, burrow dwelling is well exemplified by some members of the superfamilies Gecarcinucoidea, Goneplacoidea, Potamoidea, Grapsoidea, Xanthoidea, Grapsoidea, and Ocypodoidea (Macnae 1968, Crane 1975, Vannini 1980; for taxonomy, see Ng et al. 2008). Within these groups, many species are obligately fossorial. Burrow descriptions are best known for members of the semiterrestrial ocypodid genera Ocypode and Uca (e.g., Hayasaka 1935, Linsenmair 1967, Basan and Frey 1977, Vannini 1980, Christy 1982, Lim and Diong 2003, Chan et al. 2006). Uca burrows are usually I-, L-, or J-shaped, with dilations terminally or subterminally. The descending shaft may be either vertical or inclined (Fig. 4.6A,B). In some cases, the burrow is U- or Y-shaped. Ocypode



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Fig. 4.5. Line drawings of thalassinidean burrows (side views). (A)  Calocaris macandreae, from resin cast of burrow illustrated in Nash et al. (1984). (B) Thalassina anomala, redrawn from diagrammatic illustration in Verwey (1930). (C) Axianassa australis, from resin cast of burrow illustrated in Dworschak and Rodrigues (1997). Scale bars = 10 cm.

burrows (Fig. 4.6C,D) show a similar range of structures but are larger and may have more branch tunnels. Burrow structure in both Uca and Ocypode species has been shown to vary with location, season, sex, reproductive status, and maturity. The most complex burrows appear to be those of male Ocypode saratan that descend in a spiral (Fig. 4.6C), the direction of which is related to the handedness of the crab, and may have several subsurface galleries (Al-Kholy 1959, Linsenmair 1967, Eshky 1985). Spiral structures are also seen in some semiterrestrial Macrophthalmus species (Macrophthalmidae; Verwey

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Fig. 4.6. Brachyura burrows. (A)  Side view of Uca pugilator, redrawn from illustrations in Christy (1982) derived from plaster casts. (B) Side view of Uca inversa inversa, from photographs of plaster cast of burrow by R.J.A. Atkinson, also illustrated in Eshky et al. (1995). (C) Ocypode saratan, spiral burrow of male crab from plaster (gypsum) cast by R.J.A. Atkinson. (D) Ocypode quadrata adult burrow, from resin cast of burrow illustrated in Frey and Mayou (1971). (E) Cardisoma carnifex, from photograph of cement cast of burrow in Braithwaite and Talbot (1972). (F) Helice tridens tridens, plan view from photograph of resin cast of burrow in Ohshima (1966). (G) Helice tridens tridens, side view from photograph of plaster cast of burrow in Ohshima (1966). (H) and (I) Eriocheir sinensis, side view and plan view, respectively, from photographs of resin casts of separate burrows in Rudnick et  al. (2005). ( J)  Sudanonautes africanus, redrawn from illustrations in Bertrand (1979). (K) Goneplax rhomboides, side view, from photograph of resin cast of burrow in Atkinson (1974). Scale bars: A–K = 10 cm, approximate in case of J.

1930, Farrow 1971, Chakrabarti and Das 1983): other Macrophthalmus burrows are of simpler construction (Braithwaite and Talbot 1972, Nye 1974, Vannini 1980, Chakrabarti and Das 1983). Burrow depth appears to relate mainly to access to damp sand, from which some crabs are able to extract water, or access to standing water (Wolcott 1976, 1984). Thus, burrow depth will vary with factors such as local topography, tidal range, beach position, and sediment characteristics. Burrows of Dotilla and Scopimera are relatively simple (although showing some variation in sediments of differing granulometry) and are identifiable by characteristic patterns of feeding pellets at their openings (Ohshima 1966, Hartnoll 1973).



R. James A. Atkinson and Lucas B. Eastman

Gecarcinid burrows, typically occurring in mangrove environments, coastal forests, or among other coastal vegetation (Britton et  al. 1982), are of relatively simple structure and descend obliquely to standing water (Fig. 4.6E). They may be linear or have a spiral structure and may be large, and short side branches may be present (Hogue and Bright 1971, Bright 1977, Berti et al. 2008). Occasionally, branch tunnels may open to the surface (Herreid and Gifford 1963). Many vegetation-associated sesarmids also burrow (Micheli et al. 1991, Thongtham and Kristensen 2003, Berti et al. 2008, among many references), but detailed descriptions of their burrows are scarce. Berti et al. (2008) noted that the burrows of Neosarmatium meinerti (Sesarmidae) descended steeply and had a spacious chamber either in the middle section or terminally: some burrows had clockwise or counter-clockwise turns, and some were Y-shaped. Sesarmid burrows and those of other grapsoid crabs range from simple shafts to complex multiple-branched systems in which burrows of conspecifics may interconnect (Alexander and Ewer 1969, Basan and Frey 1977, Vannini 1980, Malan et  al. 1988). Shallow, complexly branched burrows extending mainly in the horizontal plane are constructed by Eurytium limosum and Panopeus herbstii (Panopeidae; Basan and Frey 1977). Ohshima (1966) described the burrows of Helice tridens (Varunidae) from marshy estuarine banks in Japan. Burrows varied from deep vertical shafts with a single opening to shallow branched tunnels with several openings (Figs. 4.6F,G). Differences were related to environmental conditions, including sediment composition and the depth of the water table (Ohshima 1966, Kurihara et al. 1989). Similarly, Austrohelice (= Helice) crassa, a common burrowing crab in a range of littoral environments in New Zealand including saltmarshes, mudflats, and mangrove forests, shows variation in burrow morphology in different conditions. Burrows were deeper in hot, dry weather and more complex in muddy sediments (branched with several openings) than sandier ones (simple shaft, single opening; Nye 1977, Morrisey et al. 1999). Neohelice granulata individuals created different burrows depending on sediment type (muddy or gravel) and gender, with large males creating burrows with a widened surface opening and a chamber, which was thought to improve their mating success (Sal Moyano et al. 2012). Mangrove crabs of the genus Scylla (Portunidae) also construct burrows:  these are often inclined but may be vertical, and openings (usually one) are large and distinctive (Macnae 1968, Vannini 1980, Ewel et al. 2009). Extending from marine conditions into freshwater, Eriocheir sinensis (Varunidae; see Clark 2006) is one of the best known burrowing crabs, not least because of its notoriety as an invasive species that causes bank erosion (Herborg et al. 2003, Rudnick et al. 2005, Veilleux and de Lafontaine 2007). Rudnick et al. (2005) showed that E. sinensis burrows (Fig. 4.6H,I) varied from simple tunnels with a single opening to complex, anastomosing burrows with many branches and openings. Eriocheir sinensis burrows are sometimes occupied by several crabs, each associated with a terminal chamber. When exposed to air, the lowest part of the burrow contained standing water. Detailed descriptions of the burrows of freshwater crabs are few in number. Bertrand (1979) gave details of burrow structure in the potamonautid Sudanonautes africanus. Burrows were generally I- or Y-shaped with a terminal dilation (Fig. 4.6J), but some had an additional branch opening to the surface (i.e., three openings), and some had blind-ending subsurface branches. In most burrows, the main axis was vertical or near vertical, but some were extended in the horizontal plane. The burrows of Parathelphusa spp. (Parathelphusidae) reported by Fernando (1960), cited from Vannini (1980), are simple tunnels with a single surface opening and may bifurcate. The most detailed description of the burrows of a sublittoral crab species are those for the goneplacid Goneplax rhomboides (Rice and Chapman 1971, Atkinson 1974). The simplest burrows are horizontally extended, shallow U-shaped tunnels (Fig. 4.6K). These are usually elaborated with side tunnels. A common burrow form is a T-shape when viewed in plan, with three openings, but the most complex burrows have many branches and numerous surface openings. Many crabs show plasticity of behavior such that they are facultative burrow-dwellers when conditions are appropriate. Thus, the common European shore crab Carcinus maenas (Portunidae)

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Fig. 4.7. Brachyuran crab burrows. (A) Male Ocypode saratan on sand pyramid it constructed adjacent to its burrow opening. (B) Sediment turret around burrow opening of Uca inversa inversa. (C) Burrow opening of U. inversa inversa: the smaller sediment pellets are feeding pellets discarded from the mouthparts, the larger pellets are burrow ejecta. Scale: A, pyramid height ca. 15 cm; B, C, burrow diameter ca. 2 cm. Photos by R.J.A. Atkinson (A) and courtesy of A.C. Taylor (B, C).



R. James A. Atkinson and Lucas B. Eastman

that occurs in a variety of habitats is capable of constructing burrows in the mud of estuarine banks (personal observation). The xanthid Monodaeus couchi is a facultative burrower in subtidal muddy sediments (Hughes and Atkinson 1997), although it is more commonly encountered sheltering beneath shells or stones (personal observation). Brachynotus gemmellari (Varunidae) also appears to construct burrows opportunistically (Atkinson et al. 1998). Crab species that are not normally burrow-dwelling may opportunistically use burrows as retreats, as observed in the littoral grapsid Metopograpsus messor (Eshky et al. 1995): in this case, it is not known if the burrows were of its own construction. Perhaps similarly, the invasive varunid Hemigrapsus sanguineus has been observed to occupy disused Uca pugnax burrows in an American saltmarsh (Brousseau et al. 2003). A variety of structures are constructed by crabs at their burrow openings. These include sand pyramids in the case of some ghost crab species such as male O. saratan (Linsenmair 1967; Fig. 4.7A) and O. rotundata (Ansell 1984 as O. saratan); mud chimneys, shelters, pillars, or hoods in ocypodoids and varunids such as Uca (Fig. 4.7B), Cleistosoma, and Metaplax species (Crane 1975, Zucker 1981, Christy 1988a, 1988b, Clayton 1988, Wada and Murata 2000); and barricades (Wada 1984, 1987) and mounds in Ilyoplax spp. (Wada et al. 1994, Kitaura and Wada 1996). The sesarmid Sesarma reticulatum constructs inclined chimneys at its burrow openings (Basan and Frey 1977). In the case of some Dotilla and Scopimera species (Dotillidae), chambers covered by domes of sediment pellets (“bricks”) have been termed “igloos” (Hartnoll 1973, Gherardi and Russo 2001). Igloos appear to provide a secure air-filled chamber beneath the sand (see Tweedie 1952). The function of the other surface structures constructed by crabs is variable: most appear to be connected with reproductive (by exhibiting a place of refuge to females: Christy 2007) or territorial behavior, although in some cases the function is unknown. Apart from these architectural structures, crab burrows are often surrounded by variously patterned spoil heaps of excavated sediment or by feeding pellets (Fig. 4.7C; Braithwaite and Talbot 1972, Hartnoll 1973). In some cases, feeding pellets may form distinct patterns around burrows or be associated with feeding structures such as shallow trenches (Hartnoll 1973, Crane 1975, Gherardi and Russo 2001). Burrow plugs are another category of burrow-associated structures. In the case of Uca spp., in muddy sediment, each crab cuts a precisely shaped disc of sediment from adjacent to its burrow opening with which it adeptly seals the burrow when tidal inundation threatens, or, in sandy sediment, gathers a pile of sand that is used to seal the burrow (Crane 1975, Warner 1977, Vannini 1980). Ocypode spp. may backfill their burrow openings to preserve burrow humidity in dry conditions or prevent intrusion (Vannini 1980, Eshky 1985). Gecarcinids plug their burrows to exclude rainwater and to give protection during molting (Green 2004).

FOSSIL BURROWS There is an extensive paleontological literature on burrows because these are common trace fossils (see Frey 1975, Bromley 1996); these fossils have been assigned to ichnotaxa based on morphological features. The temporal distribution of the various crustacean groups in the fossil record is summarized by Schram (1982): some have an ancient history, with representatives in the lower Paleozoic, although their affinities with later taxa are a matter of debate (Förster 1985). Interpretation of trace fossils, however, is difficult, and the time when crustacean burrows were first established is uncertain (see Byers 1982, Gingras et al. 2000). Possible crustacean ownership of some early Paleozoic burrows has been speculated, among other possibilities (Sheehan and Schiefelbein 1984, Myrow 1995, Ekdale and Bromley 2003). Larson and Rhoads (1983) have pointed out a progression from mainly superficial biogenic effects to an increase in deep-burrowing activity when Ordovician strata are compared with those from Devonian and Cretaceous times. It is clear, however, that burrow-dwelling was a well-established crustacean lifestyle during the Mesozoic era: most fossil burrows attributed to crustaceans appear to be the work of decapods, particularly thalassinideans and crabs.

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Burrow Dwelling in Crustacea The spectacular burrow of the thalassinidean A. australis (Fig. 4.5C) is a modern example of the type of spiral fossil burrow assigned to the ichnogenus Gyrolithes (see Dworschak and Rodrigues 1997), although not all Gyrolithes are attributable to crustaceans (Netto et al. 2007). Various types of thalassinidean burrows appear to be particularly common in the fossil record, including examples within the ichnogenera Ophiomorpha and Thalassinoides (see Rasmussen 1971, Bromley 1996, Pervesler and Uchman 2009). In some cases, the presence of body fossils within the fossil burrow points to its likely builder (e.g., Bromley 1967, Sellwood 1971, Neto de Carvalho et al. 2007). One of the best known fossil thalassinideans is Protocallianassa faujasi whose burrows abound in upper Cretaceous deposits, many containing well-preserved body fossils (Mourik et  al. 2005). Care needs to be exercised, however, when suggesting a connection between burrowers and burrows; for example, a burrow occupant may be an endoekete, not the burrow builder (see Bromley 1996 for a discussion of the problems associated with making causal links between body fossils and burrows). Stomatopods were present in the Paleozoic, but modern families are more recent. They are comparatively scarce in the fossil record, and most material is of Cenozoic age (Holthuis and Manning 1969, Hof and Briggs 1997, Hof 1998). Some fossil burrows have speculatively been assigned to stomatopods, for example by Monaco and Garassino (2001) from Jurassic deposits and Wroblewski (2008) from Cretaceous/Paleocene formations. There is a paucity of paleontological information on peracarid burrows:  some ichnotaxa are speculatively assigned to them as one of several possibilities. Scourse (1996) presents strong evidence that talitrid amphipods were responsible for burrows preserved in interglacial calcareous sandstones (beach deposits) in southwestern England. The earliest evidence of freshwater decapods appears to be Permian-Lower Triassic crayfish from Antarctica (Babcock et al. 1998). Burrows attributed to them are reportedly similar in structure to modern crayfish burrows. Also, Hasiotis and Mitchell (1993) suggested that Triassic freshwater crayfish constructed their burrows in the same manner as species found today, and their burrows have similar distinctive morphologies. Crayfish burrows appear to be common in Jurassic and Cretaceous deposits (Bedatou et al. 2008), including burrows interpreted as showing evidence of parental burrows with chambers for juveniles (Genise et al. 2008). Records of fossil burrows attributable to lobsters are scarce. Some Thalassinoides are attributable to glypheoid lobsters based on the co-occurrence of body fossils (e.g., Neto de Carvalho et al. 2007). Also, Pemberton et al. (1984) describe burrows attributed to a Cretaceous palinurid lobster on the evidence of the co-occurrence of body fossils. Zonneveld et al. (2002) also suggested lobsters as possible constructors of burrows from Middle Triassic deposits in Canada. Burrow traces attributed to crabs on the basis of their structure (e.g., within ichnogenus Psilonichnus), aided in some cases by the presence of body fossils, are common in Mesozoic and Cenozoic rocks (Frey et al. 1984, Gingras et al. 2000). Of particular interest is the occurrence of Middle Jurassic burrows interpreted as evidence of crabs with a semiterrestrial lifestyle (Marshall 2002). Some fossil crab burrows reported from American Quaternary carbonate deposits are interpreted as being the work of the semiterrestrial Ocypode quadrata, a species still present in the region (Curran 1984). Ohshima (1966) attributed Pliocene fossil burrows to the crab Helice based on similarity with modern burrows of these crabs.

BURROW CONSTRUCTION AND MAINTENANCE Many detailed descriptions of crustacean burrowing behavior have been published (e.g., Stevens 1929, Atkinson 1974, Crane 1975, Vannini 1980, Karplus 1987, Dworschak and Ott 1993, Atkinson et al. 1997), and it is not intended to repeat this in detail here but rather to state certain general



R. James A. Atkinson and Lucas B. Eastman

principles. Most crustaceans are excavators; that is, they remove sediment from the site of construction and deposit it elsewhere. Broadly, burrowing behavior is divisible into the following components: loosening the deposit at the site of excavation, gathering and lifting it, and then transporting it either outside the burrow, or elsewhere within it. The phases of a burrow’s construction are initial formation of a basic burrow, development of this into a “mature” burrow, and thereafter burrow maintenance. Some authors have defined more specifically the behaviors that crustaceans exhibit while burrowing and engaged in burrow-oriented activities. For example, Stamhuis et al. (1996) classified the behavior of C. subterranea into tamping, pumping, bulldozing, turning, lifting, ventilating, sitting, walking, grooming, stirring, carrying, dropping, and chopping (see Fig. 4.8; Stamhuis et al. 1996). Sediment is mined using various appendages, usually anterior thoracopods such as third maxillipeds, major chelipeds, and anterior pairs of ambulatory pereopods. Mined sediment is usually carried in a “basket” formed by anterior limbs. In stomatopods, the basket is formed by the maxillipeds (Atkinson et al. 1997). Isopods dig using their mandibles and anterior pairs of legs, and their antennae may also be used to help carry sediment (Linsenmair 2007). In the case of amphipod crustaceans, sediment gathered from the site of excavation may be carried by the anterior thoracopods; for example, gnathopods in the case of M. loveni (Fig. 4.9A; Atkinson et al. 1982). In astacidean and thalassinidean decapod species, this basket is formed by the third maxillipeds and anterior pairs of pereopods (Fig. 4.9B). Species such as lobsters (Fig. 4.9C), some thalassinideans, and alpheid shrimps may use their claws to bulldoze sediment (Karplus 1987, Nickel et al. 1995, Stamhuis et al. 1996), but mostly it is carried in the manner indicated earlier. Brachyura variously use their chelipeds and several other pereopods on the trailing side to carry sediment (Fig. 4.9D; Atkinson 1974, Crane 1975, Vannini 1980, Atkinson and Taylor 1988). Sometimes sediment is carried only by the major chelipeds (some crabs and alpheids; Alexander and Ewer 1969, Atkinson et al. 2003).

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Fig. 4.8. Schematic drawings of behavioral states of Callianassa subterranea projected on a simplified burrow. From Stamhuis et al. (1996), with permission from Elsevier.

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Burrow Dwelling in Crustacea Suspended or loose sediment may by plumed away by pleopod beating, as described, for example, in alpheids, stomatopods and thalassinideans (Fig. 4.9E; Karplus 1987, Nickell and Atkinson 1995, Atkinson et al. 1997, 2003). The amphipod C. arenarium initially probes the sediment with the tips of its second antennae before loosening sand beneath its body with its anterior appendages and flushing this from the developing burrow in a stream of water generated by the pleopods, with anchorage against the burrow wall provided by uropods and several pairs of pleopods (Ingle 1966). In some crustaceans (e.g., lobsters), the tail fan is implicated in scraping sediment (Berrill and Stewart 1973), but this method of sediment movement appears to be rare. Burrows may be lined or unlined, depending on the substratum type and the category of crustacean. If the sediment is fine-grained, then a burrow will maintain its structure without the necessity to consolidate the walls, in contrast to burrows in sandy sediment where consolidation of the burrow wall may be required to prevent collapse. Some crustaceans line their burrows with secretions, others plaster the walls with fine sediment or plant fragments or otherwise compact the burrow walls (Dworschak 1998, Kneer et al. 2008, Vonk et al. 2008). This activity has geophysicochemical implications because it influences the preservation potential of the burrow and the exchange of material across the burrow wall (Bromley 1996, Atkinson and Taylor 2005).

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Fig. 4.9. (A) Maera loveni carrying bolus of sediment in its gnathopods. (B)  Calocaris macandreae carrying bolus of sediment from its burrow using its anterior pereopods and third maxillipeds. (C) Juvenile Homarus gammarus removing excavated sediment from its burrow, partly by bulldozing with outer faces of the major chelipeds and partly by carrying sediment in a basket formed by the anterior pereopods and third maxillipeds. (D) Goneplax rhomboides transporting sediment between its folded chelipeds, supported from beneath by the second and third pereopods of the trailing side. (E) Upogebia deltaura clearing suspended sediment using its pleopods. Photos by R.J.A. Atkinson (A–D) and courtesy of A.C. Taylor (E). Scale bars = 1 cm.



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The time taken to establish a burrow will vary with the size of the burrower and the consistency of the sediment. In the case of C. subterranea held in laboratory tanks containing natural muddy sand sediment, burrowing was rapid initially, and burrow complexity increased with time, after which further increases in burrow length were small (Fig. 4.10; Stamhuis et al. 1997). The sediment expulsion rate reflected this pattern, being initially high and then declining (Stamhuis et al. 1997). Burrow maintenance is important because without it the burrow will degrade, leaving it uninhabitable or energetically expensive to repair (Stamhuis et al. 1997). The large energy investments of some crustaceans in their burrows provides the impulse to preserve these structures: an analysis of the burrowing shrimp C. subterranea held in narrow aquaria in which they burrowed in natural sediment showed that they spent approximately 27% of their time burrowing: this was interpreted as including both burrow maintenance and deposit feeding and comprised around 40% of the time that the animals were active (Stamhuis et al. 1996). In the semiterrestrial mangrove crab Ucides cordatus, burrow maintenance was the second most frequent activity after feeding (Nordhaus et al. 2009).

BURROW FUNCTION It has been seen that burrows vary from simple, shallow tunnels with a single opening to complexly branched, deeply penetrating burrow systems with numerous surface openings. Structure relates both to function and the morphology and phylogenetic history of the burrower (see Dworschak and Ott 1993, Atkinson and Taylor 2005). Deep burrows are also reported from littoral, marine, and freshwater environments (e.g., Pemberton et al. 1976, Grow and Merchant 1980, Kinoshita 2002, Richardson 2007). Deep burrows of crayfish may reflect the need to access standing freshwater, particularly during dry periods. Also, for littoral crustacean species, great depth presumably reflects the need to access damp sand or standing water when the burrow drains at low tide. In other cases, deep littoral burrows may relate to protection from predation, reduction of environmental stress, or to feeding (Kinoshita 2002): very deep burrows in sea-bed sediments (Pemberton et al. 1976) are more difficult to explain.

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Burrow Dwelling in Crustacea Refuge from Predators Most obviously, burrows provide a refuge that gives some protection from predators (Macnae 1968, Chapman 1980, Atkinson and Taylor 1988). An interesting specific example is given by Thiel (1999) who has shown that the burrows of the amphipods L. pinguis and C. bigelowi afford protection from shrimp predation to their offspring. Nevertheless, many predators are able to target crustaceans within their burrows (see, e.g., Macnae 1968, Macintosh 1979, 1982). Protection from Environmental Extremes In the case of semiterrestrial crustaceans, the burrow provides a benign environment that protects the occupant from environmental extremes. Thus, the occupant is protected from excessively high or low temperatures outside; the burrow is humid and often extends down to damp sediment or standing water, which can be used for rehydration (see Atkinson and Taylor 1988 and references therein). Locus for Molting Crustaceans are vulnerable when they molt and during the period that they remain “soft,” that is, before recalcification of their exoskeleton. During this period, crustaceans behave cryptically, with the burrow providing an ideal refuge in fossorial species (e.g., Green 2004). The timing of molting may be associated with reproduction (Adiyodi 1985). Locus for Territorial Behavior Often combined with reproductive and feeding functions, the burrow is also a territorial center that will be defended against conspecifics and other intruders (Macnae 1968). In the semiterrestrial mangrove crab U.  cordatus, observed agonistic behaviors were mainly a result of high competition for burrows (Nordhaus et al. 2009). Considering the significant effort that some crustaceans put into the creation of their burrows (see the section “Burrow Construction and Maintenance”), it is energetically costly to lose a burrow, while inhabiting an already formed burrow is energetically efficient. Many burrowing marine creatures, crustaceans included, readily inhabit burrows created by other species, and eviction from a burrow by these or conspecifics is a real threat. As well as reducing the risk of predation, this threat may be one of the factors that has led many surface-feeding crustaceans to defend their burrows. Territoriality is pronounced in the desert isopod H. reaumuri because it is highly dependent on its burrows, which can be constructed only during a specific time of the year because of desert temperatures and soil quality. It defends its burrow by using a social behavior in which it forms strictly monogamous pairs, with one partner guarding the burrow and the other leaving intermittently to forage (Linsenmair 1984). Interestingly, in two species of burrowing crayfish Parastacus spp., the primary burrower was less aggressive than the secondary burrower (Dalosto et al. 2013). Possibly this lower level of aggression in the primary burrower is due to the fact that these often share burrows with conspecifics, most likely genetically related individuals, whereas the secondary burrower has a more solitary lifestyle (Dalosto et al. 2013). Locus for Reproduction The burrow may have reproductive significance in a number of ways. Mating burrows are reported for a variety of crustaceans (e.g., Hughes 1973, Christy 1982, Green 2004). For example, in the breeding season, males of the ghost crabs O.  saratan and O.  rotundata construct



R. James A. Atkinson and Lucas B. Eastman

sand pyramids at the opening of their burrows (Vannini 1980). These act as visual signals to the females. Some fiddler crabs also create structures at the openings of their burrows that have sexual function (see also the section on Brachyura): Uca terpsichores females under predation risk preferred males that had constructed a hood at the opening of their burrows (Fig. 4.11; Christy 2007, Kim 2007). Hoods mimic various objects female crabs approach for shelter to reduce predation risk, and therefore function as "sensory traps", attracting them to the burrows of males (Christy et al. 2003). Copulation in many burrowing species, for example many Uca spp., occurs within the burrow (Macintosh 1982). The Norway lobster, N. norvegicus, is an example of a species in which the females withdraw into their burrows when ovigerous and mostly remaining there, relying on metabolic food reserves and opportunistic access to food near the burrow until the developing larvae hatch (Chapman 1980, Bell et al. 2006). Adult–juvenile associations are found within burrows of some amphipods, isopods, and decapods (Frey and Howard 1975, Basan and Frey 1977, Chapman 1980, Horwitz et  al. 1985, Tuck et  al. 1994, Thiel 1999, Linsenmair 2007). Locus for Feeding Burrows are loci from which many crustaceans emerge to forage, either in close proximity to or at some distance from their burrows. Some crustaceans never or rarely leave their burrows, and, for these, the burrow is therefore the environment in which they habitually feed. This may be by suspension-feeding, as in the case of upogebiid thalassinidean shrimps (Dworschak 1983); or, in callianassids and some other thalassinidean groups, by deposit-feeding on material subducted into the burrow or occurring within the burrow walls (Nickell and Atkinson 1995); or by caching material in burrow chambers and utilizing it either directly or when it has decomposed (Dworschak 2001, see also Atkinson and Taylor 1995). Some predatory species will take food to the burrow for later consumption (e.g., the Norway lobster [personal observation]). Some fiddler crabs may carry organic-rich sediment into their burrow in anticipation of remaining within their sealed burrows

Fig. 4.11. A male fiddler crab Uca terpsichores waving its enlarged claw to attract females near a sand hood at the opening of its burrow. Female crabs seek out this hood as refuge, thus enhancing female survival and increasing the male’s reproductive chances. From Kim et al. (2007), with permission under the Creative Commons License.

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Burrow Dwelling in Crustacea when these are immersed during spring tides: the cached sediment acts as a food source (Macintosh 1988, D.J. Macintosh personal communication). Mangrove-associated crabs may take leaf litter into their burrows (Nordhaus et al. 2009; Fig. 4.12). The sediment ingested by deposit-feeding crustaceans within their burrows or adjacent to them may have organic content derived from several sources. Using stable isotope analyses, a number of studies have shown the importance of phytoplankton, algae, seagrasses, or mangrove-derived material to thalassinidean shrimps (Boon et  al. 1997, Kinoshita et  al. 2003, Abed-Navandi and Dworschak 2005, Yokoyama et al. 2005, Shimoda et al. 2007). Palomar et al. (2004) considered the burrow-dwelling alpheid shrimp Alpheus macellarius to be a generalist, predominantly deposit feeding on organic material derived from seagrass, but also grazing seagrass epiphytes; it was also thought to take microorganisms and small invertebrates as it processed fine-grained sediment. Vonk et al. (2008) showed that A. macellarius cuts fresh seagrass leaves and caches this material within its burrow: this facilitated nutrient recycling within the seagrass meadow rather than detached leaves being exported in the current. The cached material sustains decomposer communities and provides food for the shrimp either directly or indirectly (Abed-Navandi et al. 2005, Dworschak et al. 2005). In the case of thalassinideans, a number of attempts have been made to relate burrow structure to feeding category (Suchanek 1985, Griffis and Suchanek 1991). Some schemes are more successful than others, with difficulties including that a given species may be capable of more than one type of feeding, that burrow structure for a given species may be different in different grades of sediment (Atkinson and Nickell 1995, Rowden and Jones 1995, Berkenbusch and Rowden 2000, Dworschak 2000), and that different parts of the burrow may have different functions (Nickell and Atkinson 1995). Nevertheless, within the constraints on burrow structure conferred by the morphology of the burrower, it is reasonable to suppose that burrow structure will reflect burrow function. Thus, crustacean burrows that are used as refuges are often simple:  burrows of

Fig. 4.12. Gecarcinus lateralis feeding on leaf litter beside its burrow. Carapace width ca. 6 cm. Photo courtesy of A.C. Taylor.



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suspension feeders contain one or more U-shaped elements, burrows of deposit feeders are usually complexly branched, and those that cache material have dilated galleries used for this purpose. It must be remembered, however, that different parts of burrows may have different functions. Other Burrow Functions Some species generate sounds within their burrows, for example, the ghost crab Ocypode ceratophthalmus—in this case seeming to serve as a warning to intruders that the burrow is occupied (Hughes 1966). There may also be a sexual component to sound production within and adjacent to burrows, as described for various Uca species by Salmon and Atsaides (1968). In the case of U. pugilator, the burrow was shown to amplify the sounds produced by the occupant, and Salmon and Atsaides (1968) suggested that shelters at burrow openings of some species might help direct the sounds produced by the crabs.

ECOSYSTEM ENGINEERING Burrowing crustaceans can have profound effects on their environment, and the term “ecosystem engineers” has been coined for species that exemplify such effects in both modern and ancient environments (see Jones et al. 1994, Berkenbusch and Rowden 2000, Curran and Martin 2003, Gibert et al. 2006). The following are a few examples among many that demonstrate ecosystem effects by burrow-dwelling crustaceans. Thalassinideans are important ecosystem engineers (Suchanek 1983, Flach and Tamaki 2001, Berkenbusch and Rowden 2003, Tamaki 2004, Siebert and Branch 2006, Pillay and Branch 2011), not only in terms of their bioturbation and effects on bed topography and other biota, but also on the flux of oxygen and nutrients as a result of the irrigation of their burrows (Webb and Eyre 2004, Atkinson and Taylor 2005). Considerable amounts of sediment may be reworked by crustaceans, both to the surface from where some of it may be transported elsewhere by currents, or by subsurface redistribution (Dworschak 1983, Nickell et al. 1995, Kneer et al. 2008). The ecosystem effects of such activity can be both positive and negative. An example of the latter is seen where burrow-dwelling callianassids living at high density in the bottom sediments of penaeid shrimp farms have been shown to have dramatic negative effects by exerting a heavy oxygen demand and releasing toxic compounds to the overlying water (Nates and Felder 1998, 1999, Felder 2001). Another example is where the bioturbation caused by an invasion of callianassids reworked the sediment column and transformed a sandy beach into a mud flat, with negative effects on elements of the previous biota (Tamaki 2004). Positive and negative ecosystem effects have also been demonstrated for crabs. For example, Montague (1980) suggested that the activity of Uca species in salt marshes increased carbon and nutrient flow, enhanced oxygen availability in the soil, and promoted Spartina growth, but had negative effects on algae through grazing. Botto et al. (2000) showed that burrowing crabs N. granulata altered the sediment conditions and prey behavior on southwestern Atlantic shores and suggested that this affected habitat use and feeding success of migratory shorebirds. Some birds were advantaged and some were disadvantaged by the bioturbating activities of the crabs. Botto and Iribarne (2000) showed that N. granulata stabilized estuarine shore sediment by trapping fine sediment in its burrows (open when immersed) and then adding this to the surface as burrow ejecta, whereas Uca uruguayensis (burrows closed when immersed so do not trap sediment) destabilized sediment by pelletization (feeding pellets and pellets of excavated sediment), thus increasing its erosion potential.

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Burrow Dwelling in Crustacea Within Southeast Asian mangrove forests, the thalassinidean mud lobster Thalassina anomala has a major structural effect: its large mounds of excavated sediment elevate the forest floor, provide a substratum for plant colonization, and thus promote a transition to terrestrial vegetation (Macnae 1968, Macintosh 1988). Although these processes help consolidate the coastal forest, Macintosh (1988) pointed out that the species is unpopular with farmers, fish farmers, and foresters because its burrowing activities can undermine embankments, and its mound-building interferes with mangrove tree colonization. An interesting ecosystem service provided by crustacean burrows within mangroves is described by Stieglitz et al. (2000). These authors illustrated a large complex burrow occupied by a sesarmid crab (Perisesarma messa as Sesarma messa) and an alpheid shrimp. There was evidence that such burrows prevented the buildup of salt in the soil around the mangrove roots by reduction of diffusion distance and exchange of burrow water by tidal flushing. In desert environments, the burrow-dwelling isopod H. reaumuri has been shown to promote soil erosion, return leached salts to the soil surface, increase the organic content of the soil surface via its feces, and thus affect decomposition rates, nutrient availability, and primary productivity. All are interpreted as positive effects: even the erosion improves the soil moisture regime and redistributes organic material and nutrients (Shachak and Yair 1984). A final example is provided by the abundant burrow-dwelling amphipod C. volutator. A positive ecosystem effect is that the irrigated burrows of the species oxygenate the muddy sediment of estuarine shores, which in turn increases rates of nitrification (Hylleberg and Henriksen 1980); but negative effects are that the species appears to cause sediment erosion and inhibits the establishment of the pioneering halophyte Salicornia europaea that helps consolidate estuarine shores (Gerdol and Hughes 1993, 1994).

ADAPTATIONS TO A BURROW-DWELLING MODE OF LIFE Adaptations are morphological, physiological, and behavioral and have been addressed by many authors. Therefore, the following comments are restricted to a few general observations. Crustacean limbs are ideal tools for penetrating and displacing sediment and may be modified to better achieve this (Faulkes 2013). An elongated and flexible body is well adapted to maneuvering within a burrow and is best exemplified by members of the Thalassinidea, particularly callianassids (Fig. 4.13) and upogebiids. The burrows of species whose bodies are less flexible (e.g., astacideans) are generally less complex. Burrow-dwelling crabs are often laterally elongate with a subcircular cross-section, this being reflected in the cross-section of their burrows. Physiological adaptations have received much attention. Species that habitually burrow in aquatic environments need to be able to cope with exposure to hypoxia, hypercapnia, and sulfide, conditions that are potentially hostile: adaptations are similar to those of species that experience these conditions in other habitats. In contrast, the burrow environment of terrestrial and semiterrestrial species is benign and gives the occupants essential protection from environmental extremes: most of the adaptations shown by these species have more to do with life in air than life in a burrow. These and other adaptational aspects are reviewed in Atkinson and Taylor (1988, 2005)  and Taylor and Atkinson (1991). Some species remain almost continuously within their burrows: any surface activity is restricted to burrow maintenance and feeding activity in the immediate vicinity of burrow apertures. This behavior is typical of most thalassinideans. Others habitually emerge to feed. For thalassinideans, whether or not contact between burrows of opposite sexes is established subsurface or via surface excursions between burrows is largely unknown.



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Fig. 4.13. The thalassinidean Callianassa subterranea exemplifying an elongate and flexible body that is ideal for burrowing. Scale bar =1 cm. Photo by R.J.A. Atkinson.

ASSOCIATIONS Burrows constructed by crustaceans may be occupied by other species. This relationship may be facultative or obligate, and there are many examples, only some of which are mentioned here. The best-known example of the latter is the symbiotic relationship that exists between species of goby that co-occupy the burrows constructed by alpheid shrimps (Karplus 1987). So far in this chapter, most of the burrow-dwelling crustaceans that have been considered are those that construct the burrows in which they occur. However, there are many examples of crustaceans that secondarily occupy burrows created by other species. Sometimes the builder is another crustacean, but the burrow constructor is often a member of a different group (e.g., an echiuran or a fish). Probably the best known example is of species that occupy the burrows of Urechis spp. (echiuran), a “host” which is known as the “fat inn keeper”: these endoeketes include crabs (Itani et al. 2005). Itani (2002) also reports grapsid crabs from the burrows of thalassinidean shrimps. The relationship may be facultative or obligate. Several alpheid shrimp species are reported from burrows constructed by other species (e.g., those of various echiurans), which may also harbor a variety of brachyurans including xanthiids and pinnotherids (Anker et  al. 2005). Alpheids are also reported from thalassinidean burrows (MacGinitie 1934, Dworschak and Rodrigues 1997, Dworschak et al. 2000). Somewhat enigmatically, alpheid shrimp endoeketes are also reported from the burrows of predatory stomatopods (Atkinson et al. 1997, Froglia and Atkinson 1998, Hayashi 2002). Hippolytid shrimps are reported to be associated with the burrows of tilefish, as are goneplacid crabs (Williams 1987). Richardson and Horwitz (1988) reported examples of the coexistence of two species of crayfish, their burrows being conjoined. Many species have been reported from occupied crayfish burrows (e.g., by Lake and Newcombe 1975). The burrows of some crabs also harbor many associates (Bright and Hogue 1972, Bright 1977). Members of many animal groups are associated with crustacean burrows, including polychaetes, amphipods, bivalves, carideans, and fish (Hall-Spencer and Atkinson

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Burrow Dwelling in Crustacea 1999, Kneer et al. 2008). In some cases, the burrows of different crustacean species may interconnect, as in the case of the amphipod M. loveni with the Norway lobster N. norvegicus (Atkinson et al. 1982) and in the case of some crabs (Basan and Frey 1977).

FUTURE DIRECTIONS The study of crustacean burrows has received much research attention during recent decades, with burrow-casting techniques being the main impetus, but many questions remain to be answered regarding the diverse methods of burrow construction, the diverse architecture of burrows, burrow function, the burrow environment, and the ecological effects of burrows and their occupants. Observing burrowing behaviors is obstructed by sediment, so innovative methods of studying burrowing in the field and the laboratory are needed, using modern direct and remote recording techniques to build on studies such as those of Ziebis et al. (1996, 1998), Stamhuis and Videler (1995), and Stamhuis et al. (1996, 1997). Very little is known about the behavior of many burrowing species and how they partition time and resources. For thalassinideans, very little is known about reproductive behavior. Of particular interest is the role that burrows play in conspecific interactions; for example, cases where they serve as signals for mating or agonistic rituals. More needs to be known of the role of crustaceans as ecosystem engineers and of the evolutionary consequences of this (Pillay and Branch 2011). New species of burrowing crustacean are being found each year, and others for which ecological data were lacking are found to be burrowers, providing much scope for research. Most information comes from environments that are relatively easy to access, such as littoral and shallow water sands and muds. Very little is known of burrowers from the ocean floor, and their study is costly and difficult. Last, invasive burrowing crustaceans can have important ecosystem impacts that will need to be monitored throughout the future.

CONCLUSIONS Burrows are distinguishable from borings, being formed within unconsolidated sediment, usually by means of excavation and removal of sediment. The burrowing lifestyle is common among crustaceans of many groups, especially the Stomatopoda, Isopoda, Amphipoda, Caridea, Astacidea, Anomura, Thalassinidea, and Brachyura. Burrows from these taxa are diverse, ranging from simple single-opening tunnels, through U- and Y-shaped burrows, to complexly branched structures with the main development either in the horizontal or vertical plane or a mixture of both. Trace fossils of burrows are widespread, and many are attributable to crustaceans, with modern analogues providing much information about ancient burrowing taxa. It is clear that this lifestyle was well-established in crustaceans by the Mesozoic era. Burrows have many functions for crustaceans, the principal of which is a refuge from predators. They also serve as protection from environmental extremes and as loci for molting, territorial behavior, reproduction, and feeding, among other uses. Crustacean burrowers can be ecosystem engineers, disturbing the sediment in large quantities and altering the fluxes of oxygen and nutrients throughout the ecosystem. Burrowing species have developed several morphological and physiological adaptations that facilitate their lifestyle. A good example is the elongate and flexible body of thalassinideans, enabling them to occupy and maneuver within confined spaces, and their remarkable tolerance of hypoxia. A diversity of associations have arisen between crustacean burrowers and other organisms that share their burrow: in some cases, Crustacea share burrows constructed by other species. Many questions remain regarding this crustacean lifestyle, providing a rich field for further research.



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ACKNOWLEDGMENTS We are grateful to Professor Alan Taylor (University of Glasgow), Dr. Peter Dworschak (Museum of Natural History, Vienna), and Professor P.G. Moore (University Marine Biological Station Millport) for their helpful comments on this chapter. We are also grateful to Dr.  Jim Lowry (Australian Museum, Sydney) for help with the taxonomy of Japanese talitrids.

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5 CRUSTACEANS INHABITING DOMICILES EXCAVATED FROM MACROPHYTES AND STONE

Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

Abstract Many semisessile crustaceans inhabit domiciles that they have excavated from biotic or hard substrata. This contribution provides an overview of the morphological and behavioral adaptations of crustaceans that enable them to construct and maintain these homes in a variety of substrata (e.g., algae, seagrass, wood and sandstone), reproduce, and parent their young successfully, as well as acquire food resources. Crustaceans that bore into algae or seagrass blades are typically smaller in size than those that bore into algal holdfasts, stipes or wood. Typical excavators have short, compact bodies and appendages to maneuver easily within their burrows, and strong mouthparts powered by muscular heads to effectively excavate the substrata. Many species of excavating crustaceans cohabit in heterosexual pairs to mate and reproduce. Extended parental care is also common, but is often provided exclusively by the female crustacean. Burrows serve as shelter from predators and adverse environmental conditions, and many species also feed by consuming the substratum. Other species obtain their nutrition by filter feeding within their burrows. The activities of excavating crustaceans can negatively impact the structure of the substrata and, in the case of biotic substrata, even lead to its decay and ultimately death.

INTRODUCTION Many crustaceans inhabit self-constructed dwellings other than tubes or burrows in sediment (see Chapters 3 and 4 in this volume). These domiciles may provide shelter against predators or adverse environmental conditions, guarantee access to food sources, and can aid in reproduction and the parenting of young. A self-constructed domicile, however, also requires specific investments from the crustacean in the form of construction and maintenance costs, and the lack of mobility that is 118



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associated with these dwellings may limit access to resources not present at the burrow site (e.g., food or mates). For example, many organisms require substantial time and material investments to construct their domiciles by excavating cavernicolous burrows. Thus, crustaceans living in self-constructed domiciles face trade-offs between gains (protection and food) and costs (construction and maintenance) associated with a burrowing lifestyle. Here, we examine the morphological and behavioral adaptations that enable a diverse collection of crustaceans to construct and inhabit a dwelling made from either biotic or abiotic substrata, the trade-offs faced by those that excavate these dwellings, and the direct impacts that these crustaceans can have on their environment.

DIVERSITY OF EXCAVATING CRUSTACEANS AND THEIR BUILDING MATERIALS A wide variety of crustacean taxa from the subclasses Eumalacostraca and Copepoda live within self-constructed domiciles. This chapter focuses mainly on the biotic substrata that crustaceans use as hosts, including algal holdfasts, stipes, and blades; seagrass blades; seagrass seeds; and wood. Within the Eumalacostraca, there are excavating species from the Isopoda (families Limnoriidae, Sphaeromatidae, and Holognathidae), Amphipoda (families Biancolinidae, Najnidae, Eophliantidae, Ampithoidae, Lysiannasidae, and Cheluridae), and Tanaidacea (Tanaidacae). Within the Copepoda, some species from the families Thalestridae and Harpacticidae are known to burrow into algal tissues. These crustaceans create domiciles from a wide range of building materials, including both biotic and abiotic substrata, which can be hard as well as soft. Certain crustaceans can also burrow into abiotic substrata including rock (soft sandstones), peat, and even artificial substrata such as extruded polystyrene foam (Styrofoam) (Table 5.1).

Table 5.1.  Different substrata inhabited by excavating crustaceans Crustacea Maxillopoda Malacostraca Copepoda Eumalacostraca Peracarida Amphipoda Isopoda Tanaidacae Substrata Algae blades Seagrass blades Algae holdfasts and stipes Seeds Wood Abiotic Peat Sandstone Extruded polystyrene foam (Styrofoam) Biotic

Hardness Soft Soft Hard Hard Hard Soft Hard Soft

x x

x x x

x x

x

x x x

x x x x

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone Macroalgae are an important habitat for many crustaceans, including those able to construct domiciles by “curling” the blades into nests (see Chapter 3 in this volume) or excavating burrows directly into the holdfasts, stipes, or blades of the algae. Several isopod species from the genus Limnoria, in particular, bore galleries in the holdfasts of large brown algae (Cookson and Scown 1999). An example is Limnoria chilensis, which is common along the Pacific coast of South America and excavates burrows into the holdfasts of the large bull kelp Durvillaea antartica (Thiel 2003, Haye et al. 2012). The lysianassid amphipod Parawaldeckia kidderi occurs in irregular burrows in D. antarctica holdfasts, but nothing is known about their burrowing behavior (Thiel and Hinojosa 2009). Algal holdfasts are also excavated by several groups of amphipods (e.g., many species from the Eophliantidae, Lörz et al. 2010; Najna and Carinonajna from the Najnidae, Bousfield and Marcoux 2004). A few species of ampithoid amphipods construct burrows in the stipes of large kelps. Peramphithoe stypotrupetes lives exclusively within the stipes of Laminaria setchelli, Eisenia arborea, and Pterygophora californica in the northeastern Pacific, where it excavates burrows up to 50 cm in length shared by several generations (see the section “Parent-Offspring Groups”; see also Conlan and Chess 1992, Chess 1993). Similarly, Peramphithoe lessoniophila has been observed to excavate into the stipes of the kelp Lessonia berteroana (Martin Thiel, personal observation), and Amphitholina cuniculus inhabits burrows within the medullary region of the stipes of the kelp Alaria esculenta in Europe (Myers 1974). The blades and stems of macroalgae are also excavated by several species of amphipods and copepods. Amphipods from the genus Biancolina exclusively burrow, with all records to date suggesting that they are restricted to blades from fucoid algae, and, in particular, Sargassum (Lowry 1974, Ishimaru 1996, Poore et al. 2000). The ampithoid A. cuniculus is also known to excavate into blades of the fucoid Bifurcaria bifurcata in addition to kelp holdfasts (Gestoso et  al. 2014). The eophliantid amphipod Bircenna macayai inhabits small burrows in the thick thalli of the fucoid Carpophyllum maschalocarpum (Lörz et  al. 2010). Several species of copepods burrow into the blades of red and brown macroalgae, causing pinhole disease in economically important species (e.g., Undaria pinnatifida in algal aquaculture; Ho and Hong 1988, Shimono et al. 2004, Park et al. 2009; see the section “Ecological and Economic Importance”). Isopods from the family Limnoriidae, Limnoria and Lynseia, as well as amphipods from the family Najnidae have specialized members that excavate burrows into the leaves of seagrasses (Cookson and Lorenti 2001, Gambi et al. 2003, Brearley et al. 2008). Not only do these specialized crustaceans burrow into seagrass, whether it be the blades, sheathes, or rhizomes, but, in many cases, the borers also consume the living tissue that they burrow into (see Gambi et al. 2003 for a summary of seagrass borers). Reports of plant consumption by tanaids are rare, but the tanaid Zeuxo sp. bores into the seeds of the seagrass Zostera marina and Z. caulescens in Otsuchi Bay in Japan, consuming the seed tissues (Nakaoka 2002; see also the section “Ecological and Economic Importance”). The sphaeromatids and limnoriids, the latter of which are commonly referred to as “gribbles,” are the most economically important and well-known wood-excavating crustaceans because of the reported damage that members of these families have caused to both mangrove forests (Svavarsson et  al. 2002)  and man-made structures (Ray 1959). A  well-studied example is that of the wood-excavating isopod Sphaeroma terebrans that inhabits aerial roots of the red mangrove Rhizophora mangle (Perry and Brusca 1989, Thiel 2001). This is an ideal, stable habitat for the isopods because at high tide the aerial roots are frequently flushed with water (Thiel 1999a). Sphaeroma terebrans even reproduce within their burrows (see the section “Sharing of Dwellings”). Limnoriid isopods also excavate into mangrove roots (Ellison and Farnsworth 1990)  and dead mangrove wood (Cookson et al. 2012). Several other wood-excavating crustaceans have also been observed to bore into dead wood (Menzies 1957), wood impregnated with preservatives (Cookson and Barnacle 1987, Cragg and Levy 1979), and bamboo (Richardson 1909).



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

Although the excavating sphaeromatids are common in tropical and subtropical waters, limnoriids have a wider range, occurring in both tropical and temperate waters (Cragg et al. 1999). Limnoria lignorum and L.  borealis reach Arctic latitudes (Pillai 1967, Svavarsson 1982, respectively), where they have been shown to be relatively resistant to freezing temperatures (Nair and Leivestad 1958). Despite being limited to tropical waters, sphaeromatids are euryhaline and so are able to inhabit brackish waters, and certain species, including S. terebrans can even tolerate freshwater, whereas limnoriids are notably absent from intertidal mangrove systems with high freshwater input due to their lack of tolerance for lower salinities (Cragg 2003). A lesser known family of wood-excavating crustaceans is the chelurid amphipods who have a more limited geographical distribution (Pillai 1967), mostly occurring in temperate and subtropical waters (Cragg 2003), even though they also have been observed to occur in the subarctic zone (Nair and Leivestad 1958). Chelurids prefer to burrow in soft wood or in substrata already weakened by other excavating organisms (Kühne and Becker 1964). Most known wood-borers inhabit shallow waters (Cookson 1990), with an exception being Limnoria emarginata, which is known from wood falls in the deep sea (Kussakin and Malyutina 1989). Sphaeromatid isopods also excavate in a variety of abiotic substrata. Sphaeroma wadai excavates burrows in soft sandstone (Murata and Wada 2002). These burrows have particular importance during reproduction because females mate and incubate their offspring in their burrows. Other sphaeromatids also burrow in soft stone, peat, and even into extruded polystyrene foam (Brooks and Bell 2001, Davidson et al. 2008). Sphaeroma quoianum, for example, has often been reported to excavate galleries in polystyrene floats under docks (Davidson et al. 2013).

LIFE IN SELF-CONSTRUCTED DWELLINGS Morphological Adaptations For crustaceans to effectively excavate burrows in a wide variety of substrata, there are certain morphological adaptations needed. Some of these adaptations are common across the subclasses. Size and Coloring The size of an individual crustacean influences the substratum that it can burrow into. Large individuals may not be able to burrow into a material if the dimensions of the substratum are too small to accommodate the crustacean. Small individuals may not have the strength to excavate into hard or fibrous substrata. Crustaceans that burrow in algal or seagrass blades, rather than the large holdfasts, need to be small in size if the blade is to provide enough space for the crustaceans to construct a burrow and live, often not alone, within the constraints of the blade. Reports of amphipods and isopods excavating macroalgae are almost entirely confined to larger species of brown algae from the orders Laminariales (kelps), Durvilleales, and Fucales. In contrast, the smaller mining copepods have been reported from the kelps, but also from smaller algae such as brown alga Dictyota dichotoma (Shimono et al. 2004) and the red alga Rhodymenia palmata (Harding 1954). Many isopods and amphipods that excavate burrows are too large in size to burrow into individual blades of algae or seagrass and thus burrow into algae stipes and holdfasts and seagrass leaf bundles, as well as into wood, among other substrata (Pillai 1967, Brearley et al. 2008, Lörz et al. 2010). The exceptions include the mining copepods, isopods from the genus Lynseia that burrow within seagrass leaves (Brearley and Walker 1995), and amphipods from the families

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone Eophliantidae and Biancolinidae. For example, B. macayai, an amphipod 2.6 mm in length, is small enough to build burrows that traverse the thick blades of the seaweed C. maschalocarpum (Lörz et al. 2010). Biancolina, at a similar size, burrows into blades of Sargassum, but the burrows run lengthwise (i.e., parallel to the main axis of the blade) with the burrow diameter almost equal to the blade thickness (Alistair Poore, personal observation). Once the burrow is complete, the sides become eroded and blades end up with a slot removed from their central region. In contrast, the wood-excavating S. terebrans, with an average size of 6–10 mm (Thiel 1999a), may not be able to excavate into most leaves. Comparatively, adults of the copepod D. fodiens, which have an average length of only 0.6–0.7 mm, burrow into the thalli of the seaweed D. dichotoma, which are only a few cells thick (Shimono et al. 2004). The color of an excavating crustacean is often reflective of what it feeds on. Burrowing amphipods from the genera Biancolina, Bircenna, and Amphitholina all closely match the yellow-brown color of the brown algal hosts (Lörz et  al. 2010, Gestoso et  al. 2013). In general, whereas the algae- and seagrass-borer species of the Limnoriidae are white or greenish-yellow in color, the wood-excavating crustaceans of the same family are darker in color and have a reticulate pattern (Cookson 1990). The darker color may also reflect the degree of sclerotization of the exoskeleton, with species that burrow into hard substrata requiring a harder exoskeleton, which is more sclerotized, especially at the tips of the mouth parts. Short, Compact Body Shape and Appendages Crustacean excavators from several unrelated families (including the amphipod families Ampithoidae, Biancolinidae, and Eophliantidae and the isopod families Limnoridae and Sphaeromatidae) characteristically have cylindrical, stout bodies and more compact appendages (Fig. 5.1). As noted by Myers (1974), when discussing the resemblance of A. cuniculus to amphipods in the family Eophliantidae, these similarities likely result from convergent evolution due to a shared, burrowing lifestyle. A more elongated body would make it more difficult for a crustacean to navigate its burrow, and longer appendages may increase the size of the burrow that the crustacean would have to excavate to be able to provide sufficient “leg room” for the appendages. Limnoriid legs vary in length, with pereopods 1 and 7 being the longest. These are normally directed forward and rearward, respectively, with the middle pair of legs directed laterally (S. Cragg, personal observation). Lörz et al. (2010) argue that short pereopods, specifically, help to keep the overall shape of the crustacean more compact, thus minimizing the volume of substratum that needs to be excavated when creating a burrow. Crustaceans have been observed, after all, to only excavate the minimum amount of space needed. Brearley and Walker (1995) reported that the burrow formed by the isopod L. annae in seagrass blades is only slightly wider than the isopod itself. The burrow of Limnoria tripunctata was also observed to be of equal diameter to the limnoriid’s length, allowing it to easily maneuver within its domicile (Sleeter and Coull 1973). Muscular Head and Strong Mouthparts To be able to effectively excavate into algae and wood, strong cutting mouthparts, comprising mandibles, maxillae, and maxillipeds, are needed. The amphipod A. cuniculus, for instance, has mouthparts that are both prognathous and styliform (Fig. 5.1B; Myers 1974), characteristics that ensure that the amphipod has a strong bite and is well-suited to excavate into smaller crevices. Well-developed muscles are needed to control and power the cutting mouthparts, becoming evident in the voluminous heads of many excavating crustaceans, such as in the amphipod B. macayai



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

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Fig. 5.1. Lateral depictions of excavating crustaceans. (A) Peramphithoe stypotrupetes, from Conlan and Chess (1992), with permission from The Canadian Museum of Nature. (B) Amphitholina cuniculus, from Myers (1974), with permission from Royal Irish Academy. (C)  Carinonajna longimana, from Bousfield and Marcoux (2004), with permission from Amphipacifica. (D)  Biancolina brassicacephala, from Lowry (1974), with permission from Wiley. (E) Bircenna macayai, from Lörz et al. (2010), with permission from Journal of Marine Biological Association of the United Kingdom. (F) Sphaeroma terebrans, from Loyola e Silva (1960).

(Fig. 5.1E) or in most limnoriid isopods (Fig. 5.2A; Cookson 1990). Members of the amphipod family Eophliantidae are also characterized by having strongly rotating, spheroid heads (Lörz et al. 2010). The strong rotating heads are said to aid the mouthparts, especially the flattened incisor, in effectively shaving algal tissue during burrow construction (Barnard 1972). Mandibles Adapted to the Substrata The mandibles of an excavating crustacean are indicative of the specific material that the crustacean is excavating into and also the purpose of the excavating. Many excavating species, including limnoriid isopods and eophliantid and biancolinid amphipods, have anteriorly projecting mandibles that are able to excavate forward into a burrow (Fig. 5.2A; Lowry 1974). In the species of Sphaeroma and Limnoria that burrow into wood, the differentiated mandibles serve as a “rasp-and-file” combination

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Fig. 5.2. Scanning electron microscope image of (A)  the cutting mouthparts, bulbous head, and short antennae of the isopod Limnoria quatripunctata. (B) Teeth and (C) posterior with spines of the isopod Limnoria sellifera. Courtesy of Simon Cragg.

to aid with the excavation (Henderson 1924). The mandibles of S. terebrans have incisors with two unequal teeth on the right process and one tooth on the left, and also square molar processes with shallow grooves used as grinding surfaces (Si et al. 2002). The incisors of sphaeromatids, such as S. terebans, are blunter than the toothed-edge incisor on the right appendage of Limnoria (Quayle 1992). The sharp-pointed incisor of Limnoria is used to scrape off wood slivers that are small enough to ingest (Si et al. 2002). The incisors pass across each other during biting, with their corrugated surfaces moving across each other, so there is a combination slicing and grinding action (Fig. 5.3; Simon Cragg, personal communication). In contrast, S. terebans does not ingest wood, and so the blunter incisors, used for cutting larger shavings during burrow construction, suffice. Sphaeroma quoianum uses its mandibles to construct burrows in wood, sandstone, or even plastic, tearing into the substratum and shaving off smaller particles that its beating pleopods subsequently wash away (Rotramel 1975a). To avoid the wood shavings getting trapped in the setal brushes of the isopod’s first three pairs of pereopods, these shavings are released near its midsection (Rotramel 1975a). Many species have teeth and strong comb spines located on the dorsal and posterior body surface, as well as the appendages (e.g., uropod, pleotelson), as observed by Lowry (1974) in Biancolina brassicacephala and Myers (1974) in A.  cuniculus. Many wood-boring limnoriids have similar teeth and spines (Fig. 5.2B,C), which may aid in firmly anchoring the small crustaceans in their burrows during excavation activity. Behavioral Adaptations Construction and Maintenance of Dwellings Substratum Selection and Construction Many factors will impact how excavating crustaceans choose the specific microhabitat in the substratum and how they will proceed to construct their burrow. Food availability and safety from predators, as well as from adverse environmental conditions such as wave action, are likely factors that influence site selection behavior.



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

Fig. 5.3. The mandible of the isopod Limnoria quadripunctata. Courtesy of Simon Cragg.

As an example of how an excavating crustacean proceeds to select its substratum, the antennae of limnoriid isopods are not positioned in a streamlined manner when swimming, but are forward-facing, suggesting an important role of chemoreception in site selection (Henderson 2000). Limnoria uses its second antenna to frequently touch the wood prior to building a domicile (Henderson et al. 1995), indicating that chemoreception is likely to be involved in identifying a suitable burrow site. The chelurid amphipod Tropichelura gomezi, which occupies excavated burrows, also identifies a suitable domicile by probing burrow entrances in search of an unoccupied gallery (Thomas 1979). When initially constructing their domiciles, excavating crustaceans are vulnerable to predators. Choosing a softer substratum would reduce the time taken to enter the substratum, but is likely to involve reduced substratum stability and may be associated only with those species that do not live in a burrow for a significant period of time. Limnoriid and sphaeromatid isopods mostly prefer soft wood that is easier to excavate than hard woods, although, L. quadripunctata, L. saseboensis, and L. indica are species that have been found to burrow in dense hardwoods (Cookson and Scown 1999). This preference for softer woods may be because these isopods are comparatively mobile, not permanently associated with their homes (Si et al. 2000). It is likely that an individual excavates several burrows during its lifetime. Consequently, the isopods seem to favor substrata that require a shorter construction time, trading off on the durability of their self-constructed burrows. Sphaeroma terebrans, for instance, can burrow deeply enough that only their dorsal surface is exposed after one tidal cycle (Brooks and Bell 2001). This time cost is similar to species excavating into algal blades; amphipods are able to burrow into the thallus of an alga within 2 h (Gestoso et al. 2013). Burrowing speed may also depend on the age and size of the individuals: subadult S. terebrans

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone were substantially faster in establishing their own burrows in mangrove aerial roots than were small juveniles of this species (Thiel 2001). Despite most wood-excavating limnoriids preferring softer wood, the species of Limnoria that excavate into Macrocystis kelp holdfasts are often found in older and more fibrous holdfasts ( Jones 1971). The large numbers of limnoriids in older holdfasts may not only be due to their larger size, but also because of the more hardened tissue ( Jones 1971). Thus, the tougher tissue will result in a more durable and structurally sound burrow. As with other herbivores that consume algal and seagrass tissues, selection of burrow sites for those species that also consume their hosts will involve selection among the species available in the local environment and among tissues within the chosen host. These choices will be influenced by the toughness of tissues, food quality (see the section “Food Resources”), and by potentially deterrent secondary metabolites present in algal and seagrass tissues. Distributional data suggest that those crustaceans that excavate algal blades are highly selective among available algal species (e.g., Biancolina restricted to Sargassum; Poore et al. 2000), and burrows are frequently unevenly distributed among plant tissues within a species. Bircenna macayai create only one or two openings in the meristoderm layer of C.  maschalocarpum stems to excavate its burrow (Fig. 5.4; Lörz et  al. 2010)  As the copepods D.  fodiens and Dactylopusioides malleu burrow into their hosts, the epidermal layers remain uneaten, so that the cell wall will provide protection for the burrow (Shimono et al. 2004, 2007). Similarly, the isopod leaf miner L. annae burrows through the mesophyll, but leaves the cuticle and epidermis of seagrass blades intact (Brearley and Walker 1995). The burrows were generally not near the margin of the

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Fig. 5.4. (A) The brown alga Carpophyllum maschalocarpum, which hosts burrows of the amphipod Bircenna macayai. (B) The anterior and (C) posterior view of B. macayai in an excavated burrow. Photo by M. Martin Thiel.



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

leaf, which may not be as structurally supportive as the center of the blade. Unfortunately, experimental studies on these algal-excavating species are rare, and we lack a general understanding of what tissue traits (toughness, nutritional, or chemical) determine burrow site selection (although see Gestoso et al. 2014 for substratum selection experiments with the amphipod A. cuniculus). Limnoria has been observed to prefer wood that is already colonized by microorganisms, which would indicate that the substratum is nutritionally enriched (Henderson and Cragg 1996). It is important to excavating limnoriids for the wood to be colonized by bacteria and fungi because these isopods also feed on these wood degraders. Certain species of excavating crustaceans are not efficient borers; to minimize the time spent outside burrows and vulnerable to predators, they will identify damaged substrata that are easier to penetrate. For example, chelurids avoid being attacked by predators on the exterior of wood by commonly settling on wood that limnoriids have previously burrowed into but have abandoned (Pillai 1967). Tropichelura gomezi was observed to enlarge the limnoriid burrows into large, unroofed galleries, taking advantage of the softer wood in the interior of the already-excavated burrow (Thomas 1979), although Chelura terebrans are also able to live and reproduce independently, by excavating grooves into soft wood (Cragg and Daniel 1992). Burrowing may also be facilitated or impeded by other organisms. Peramphithoe stypotrupetes excavates into stipes of L. setchellii that have already had laminar tissue layers removed by gastropod grazers (Chess 1993). This observation indicates that P. stypotrupetes is most likely not capable of making the initial excavations into the lamina or outer stipe tissues (Chess 1993). The isopod Limnoria clarkae was found to establish burrows in clean aerial roots of mangroves, but when roots were overgrown by fouling organisms such as ascidians or sponges, burrowing was impeded (Ellison and Farnsworth 1990). Maintenance Once a domicile is constructed, it provides protection from environmental conditions as well as predators. The substrata may also provide food for the crustacean or be where it reproduces and cares for offspring. So it is important to be able to maintain the burrow sufficiently for these activities to take place. The burrowing in seagrass by different excavating crustaceans initially leaves the outer sheath face epidermis intact, as protection, but as the burrowing advances, the epidermis is often damaged (Tussenbroek and Brearley 1998). The damage may be a result of wear or higher densities of isopods living within the burrow. The wear and tear of a burrow will often result in individuals leaving a damaged burrow and constructing a new burrow. The size of burrows, methods used to construct them, and numbers of individuals per burrow all hint at the length of time crustaceans are likely to occupy a given burrow. For example, in order to ensure that the epidermal layers provide sufficient protection but still be able to get enough sustenance by feeding on the algae, copepods D. fodiens excavate new burrows every few days (Shimono et al. 2004). In contrast, amphipods such as P. stypotrupetes, which excavate large chambers in kelp stipes, and copepods, such as D. macrolabris and D. fodiens, remain in one burrow for a significant period of time, even brooding in the burrow (Conlan and Chess 1992, Shimono et al. 2007). Most species will live in a domicile, albeit not the same one, for all life history stages. An exception is the copepod D. malleus, which creates a dome-shaped capsule of mucus while in the burrow and later lives on the surface of the algal tissue for their adult stages (Shimono et al. 2007). A major benefit of burrow-living exemplified by the use of the capsule is the protection that it provides. The capsule is used within the burrow for protection during metamorphosis and also on the surface to shield against hydraulic action and predators (Shimono et al. 2007). Unfortunately, detailed behavioral studies that quantify burrow residence times and the factors influencing the departure of individuals from burrows are lacking. For those crustaceans that make

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone nests by curling algal fronds (see Chapter 3), nest maintenance and residence times are influenced by the rapid growth rates of kelp blades. For example, the kelp curler P. femorata is able to exploit the growth pattern of the kelp blades Macrocystis pyrifera to prolong its residence time (Cerda et al. 2010). Ventilation To remain healthy and be able to function within a domicile, crustaceans must ensure ventilation of both water and oxygen throughout the burrow, renewing the water in contact with the crustacean’s pleopods as required for respiration (Henderson 1924, Rotramel 1975a). Many different species of crustaceans, across substrata, have been observed to make small holes in their burrows every few millimeters to ensure sufficient oxygen supply and adequate water circulation. Examples of this include the isopod Limnoria simulata that burrows into the sheath of the outer foliar leaves of seagrass shoots (Tussenbroek and Brearley 1998) and the wood-excavating limnoriids (Pillai 1967, Sleeter and Coull 1973). The extensive burrows of P. stypotrupetes also have numerous openings to the outside (Conlan and Chess 1992), contributing to the efficient ventilation of these dwellings that can be inhabited by more than 200 family members. To actively ventilate burrows, crustaceans also frequently beat their pleopods, as observed, for example, in B.  macayai (Fig 5.4; Lörz et al. 2010). Food Resources The main purpose of a burrow to an excavating crustacean is as shelter from predators and unfavorable environmental conditions. Many species are herbivores that ingest the tissues of biotic substrata, although this behavior can pose the problem that feeding activities also lead to the destruction of the domiciles. Other crustaceans living in self-constructed domiciles seek alternative food sources using a variety of methods that are outlined here. Consumption of algal tissues from within burrows into stipes and holdfasts has been observed in limnorid isopods ( Jones 1971) and in amphipods from the families Eophliantidae (Lörz et al. 2010), Biancolinidae (Alistair Poore, personal observation), and Ampithoidae. This latter family is predominantly herbivorous (host use reviewed in Poore et al. 2008), but only three species are known to excavate burrows and feed internally. The few species of excavating copepods also feed and subsist on the living tissues from within the burrows that they excavate from algae blades. For example, species within the harpacticoid copepod genus Dactylopusioides are obligately endophagous in host macroalgae (Shimono et al. 2007). Dactylopusioides malleus, endemic to central Japan, burrows into the dictyotalean brown algae D. dichotoma, only eating this algal tissue for all of its life history stages (Shimono et al. 2007). Seagrass-excavating isopods may either consume living or dead seagrass tissues. In the case of Limnoria mazzellae, dead tissues of the sheath of Posidonia oceanica, including the sheath mesophyll and epidermis are consumed (Gambi et al. 2005). Limnoria mazzellae is able to feed on the younger and relatively tougher sheaths because its mouthparts are well-adapted to feeding on the tougher substratum. Isopods of the genus Lynseia consume the mesophyll of Posidonia leaves as they excavate their burrows (Brearley and Walker 1995). The wood-excavating Limnoria ingest and metabolize the wood from within their burrows. No symbiotic microflora has been located in their digestive tracts, so it has been suggested that Limnoria produce their own enzymes that degrade the wood, thus enabling the isopod to extract nutritional value from the wood (Cragg et al. 1999). King et al. (2010) revealed that L. quadripunctata secretes key glycosyl hydrolase family 7 and 9 genes from the hepatopancreas that aid in the digestion of lignocelluloses. There is also current interest in these enzymes that extends beyond understanding Limnoria; glycosyl hydrolases may serve to convert solid biomass to liquid biofuels (Kern et al. 2013).



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

For crustaceans that ingest wood, the problem of its low nutritional value (in particular, low nitrogen content) may be resolved by the ingestion of microorganisms associated with the wood itself, with the surface of their own exoskeletons, or even from feces that have been colonized by bacteria (Becker 1971, Cragg and Daniel 1992, Cragg et al. 1999). Cookson and Cragg (1991) have also suggested that the concave nature of the abdominal segments and lateral crests of Limnoria cristata may promote the accumulation of debris and bacteria, thus providing a larger collection area. The comb setae on the pereopods of limnorids are also suitable for collecting debris, as observed in Figure 5.5A. During its grooming process, the crustacean can transfer bacteria removed from its exoskeleton and antennae to its mouth (Fig. 5.5B; Henderson 2000, Cragg 2003).

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Fig. 5.5. (A) Debris collected on the comb setae from a pereopod of the isopod Limnoria quadripunctata, courtesy of Simon Cragg. (B)  Accumulations of bacteria in the region of mouth opening for the amphipod Chelura terebrans, from Cragg and Daniel (1992), with permission from International Research Group on Wood Preservation.

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone Unlike Limnoria, most wood-excavating sphaeromatids, such as S. quoianum and S. terebrans, do not ingest the wood from their burrows, but obtain their food by filter feeding. The wood is used for protection purposes only, and these isopods filter feed from within their burrows by generating currents with their pleopods. When the current passes underneath their heads, these isopods use the plumose setae on the first three pairs of pereopods to collect the particles in the current. The plumose setal brushes are then cleaned of the trapped particulate food matter by the maxillipeds (Rotramel 1975a, Si et al. 2002). The long setae are ideally suited to transfer particles to the mouth (Si et al. 2002). Rarely do excavating crustaceans use mucus capsules, but, when utilized, they provide both protective coverings (see the section “Construction and Maintenance”) and a surface from which to feed (Hicks and Grahame 1979). For example, the mucus secreted by D. nobilis attracts and traps marine prokaryotes as well as other organic materials that the copepod subsequently ingests. Sharing of Dwellings Many excavating crustaceans do not live alone in their domiciles, sharing them with a mate for reproductive purposes and later offspring to engage in extended parental care. In certain cases, aggregations of conspecifics and even different species have also been observed to cohabit. Heterosexual Pairs Many species of excavating crustaceans cohabit in heterosexual pairs in order to be able to mate and reproduce within the safety of the burrow, including several species of Limnoria and Sphaeroma (Menzies and Widrig 1955, Murata and Wada 2002). Heterosexual pairs have been observed across several substrata (algae, seagrass, and wood domiciles). In the case of the wood-excavating isopods from the genus Limnoria, aggregations of individuals of both sexes are observed when wood is located, but they do not copulate until a burrow is properly excavated. Thus, the aggregation of the isopods facilitates reproduction when the individuals are ready to mate (Menzies and Widrig 1955, Johnson and Menzies 1956). Delaying copulation until a burrow is fully excavated would ensure that the pair is safe from predators, with Menzies (1954) observing that two individuals were only present in a burrow when that burrow was large enough to fully enclose both individuals. Adult Limnoria can be paired in burrows for more than 10 months (Cragg 2003), whereas in other species, heterosexual pairs may exist for only a short period of time, with the male often not involved in any parenting (see the section “Parent–Offspring Groups”). The seagrass-excavating L.  simulata were found to occupy burrows in pairs 40–50% of the time (Tussenbroek and Brearley 1998). Sphaeroma wadai males only accompanied the females from November to July, when the females were not yet carrying eggs (Murata and Wada 2002). There is even indication that, during the first months of the reproductive season, the large males pair with the largest (most preferred) females and later also pair and mate with the smaller females in the population (Murata and Wada 2002). In most cases where heterosexual pairs were observed, the behavior of males and females was consistent, with the female occupying a deeper region of the burrow than the male (e.g., Thiel 1999a). The relative location of the males to the females could be because the females are generally larger in excavating crustaceans and so are better equipped to carry out the excavation process. This is the case of the isopod Lynseia annae that mines seagrass (Brearley and Walker 1995) and the wood-excavating L. tripunctata, in which the female does most of the burrow construction (Sleeter and Coull 1973). Furthermore, during extended parental care, the females shield their offspring, which are occupying the interior-most sections of the burrows (Thiel 1999, 2003). The position of males close to burrow entrances could also result from mate-guarding behavior on behalf of the males. In the sandstone-excavating S. wadai, males are positioned above the females in outer parts of the burrows, with Murata and Wada (2002) suggesting that this positioning implies



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

that males select their mates and are engaged in mate guarding. The mate guarding can last for 5 months and is apparently aimed at exclusion of male competitors (Murata and Wada 2002). Parent–Offspring Groups After copulation, excavating crustaceans have different morphological and behavioral adaptations to ensure the survival of their young. Many excavating crustaceans (e.g., amphipods and isopods) carry their young in a brood pouch until the juveniles have reached an advanced development stage. After juveniles have emerged from the brood pouch, the parents may either let the offspring fend for themselves or extend their parental care. Peracarid crustaceans, which include isopods, amphipods, and tanaids, have ventral brood pouches that the eggs are shed into, facilitating the development of their young ( Johnson et al. 2001). By supporting the development of their young in a brood pouch, the young are protected when most vulnerable. The young are at a more advanced stage, generally fully developed juveniles, when leaving the brood pouch, and thus, more capable of surviving and looking after themselves, albeit their capacity to excavate in hard substrata is limited. In the wood-excavating crustaceans, the brood pouches of chelurids and limnoriids are formed by four pairs of overlapping oostegites, whereas in sphaeromatids, the brood is incubated internally and the oostegites only cover the gonopores (Pillai 1967). The brood size of excavating crustaceans varies; Brearley and Walker (1995) observed only 1–4 eggs within the brood pouch of the seagrass-dwelling Lynseia annae, and Cookson and Lorenti (2001) reported three eggs for L. mazzellae, which burrows in the sheaths of P. oceanica. Limnoria chilensis produce a reported maximum of 19 eggs per brood (Thiel 2003), and 120 embryos were reported in a P. stypotrupetes (Chess 1993). As mentioned earlier, males are rarely involved in the upbringing of the offspring, leaving parental care to the females. This has been observed in isopods and amphipods, as well as in copepods. The females of S. terebrans, for example, without males present, cared for their offspring for approximately 40 days by providing shelter (Thiel 2001). The length of parental care may depend on the stability and size of the burrow (Thiel 1999a): a small burrow, for example, would not be able to accommodate grown offspring or multiple broods. After this time period, the offspring may initially start their own burrows from the protection of their parental burrow because the offspring are not able to build their own burrows efficiently, as observed in S. terebrans (Thiel 2001) and in the young L. annae (Brearley and Walker 1985). The small juveniles may not yet have sufficient power to excavate into the relatively hard substrata quickly. By starting to excavate from the parental burrow, the juveniles are afforded the luxury of a safe environment to begin constructing their own domiciles. It will also be easier for the juveniles to excavate in the softer, interior tissue of the host rather than having to start burrowing from the cell wall or epidermis. Similar behavior is observed in L. chilensis, in which juveniles remain in the maternal burrow and grow to subadult sizes before starting their own burrows (Fig. 5.6; Thiel 2003). Extended parental care may be very efficient for the survival of offspring, with the number of developing juveniles similar to the number of brood-pouch embryos in similar-sized females (Fig. 5.8). Juveniles of L. tripunctata and L. lignorum excavate their own burrows from the parental burrow immediately after leaving the brood pouch (Henderson 1924, Johnson and Menzies 1956). The parents excavate deeper into the wood, so that subsequent broods are separated from the previous brood (Johnson and Menzies 1956). The copepod Thalestris rhodymeniae is able to take advantage of space created when it excavates into the thallus of the algae R. palmata for reproduction purposes. Rhodymenia palamata reacts to the excavation by producing galls, raising the tissues surrounding the burrow. The added space is consequently used by the copepod to reproduce and hatch its young (Harding 1954). The most striking example of parent–offspring grouping from the excavating crustaceans comes from the amphipod P. stypotrupetes, in which parents cohabit in their burrows in the stipes of kelp with up to three successive broods (Fig. 5.7; Conlan and Chess 1992). It is only when the stipe has

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Fig. 5.6. Parental care exhibited by the isopod Limnoria chilensis in holdfasts of the kelp Durvillea antarctica. (A) Burrows extending upward within the holdfast tissue. (B) Female in burrow with small juveniles at the terminal end. (C) Larger juveniles that have excavated side burrows originating from the maternal burrow. From Thiel (2003).

been either hollowed out or starts to decompose that the entire family evacuates, and the adult offspring begin to excavate their own burrows (Conlan and Chess 1992). Living with several broods requires advanced social behavior on the part of this amphipod and is not very common among burrowing crustaceans. Overcrowding within a domicile or even a substratum is likely to induce individuals to leave that substratum and initiate burrows elsewhere. The departure of juvenile L. lignorum from the parental substratum has been suggested to result from overcrowding ( Jones 1971), whereas in L. tripunctata, it is the adults that are most likely to leave the wood when overcrowded ( Jones 1971). Conspecific Aggregations There are a few known examples in which members of a species cohabit within a burrow or a large excavated dwelling, but the population structure of these conspecific assemblages has not yet been investigated. For example, the excavating amphipod P. kidderi lives in a single gallery on the holdfasts of D. antarctica with tens of other individuals (Thiel and Hinojosa 2009). Interspecific Associations Not only have crustaceans of the same species been found to share burrows, but also crustaceans of different species. Heterosexual pairs of snapping shrimps often cohabit with other species, for example, with crabs (Silliman et al. 2003), other snapping shrimps (Boltaña and Thiel 2001), and even with fishes (Karplus 1987). Most of these associations between shrimps and similar-sized organisms are found in burrows established in soft sediment or rock rubble, and, to our knowledge, there are no similar examples of crustaceans burrowing into macrophytes sharing their domiciles with organisms of similar size. There are, however, several examples of smaller associates inhabiting the burrow with an excavating crustacean or, in certain situations, living on the crustacean itself. Iais californica, a small



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

Number of offspring/female

20 16 12 8 4 0 2.0

3.0

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Fig. 5.7. The positive relationship between the number of offspring (embryos/juveniles) and body length of female Limnoria chilensis. Circles: embryos from the marsupium; squares: small juveniles from the terminal end of the maternal burrow; stars: large juveniles in side burrows. The arrow represents the number of larger offspring in a maternal burrow of a specific size; the fact that the offspring number matches the relationship of female size to embryo size in the marsupium indicates none to minimal offspring mortality. From Thiel (2003).

isopod, lives exclusively in association with S. quoianum, which provides Iais with shelter as well as food particles (Rotramel 1975b). The associate I. californica collects food particles from between the legs or on the maxillipeds of Sphaeroma when its host is filter feeding. Whereas I. californica relies on S. quoianum for its nutrition, Rotramel (1975b) was able to show that S. quoianum is not dependent on I.  californica. Burrows of L.  borealis are inhabited by the janirid isopod Caecijaera borealis, the adults of which reach about the size of juvenile Limnoria (Svavarsson 1982). A similar association had been described between the eyeless C. horvathi and its host, Limnoria sp. (Menzies 1951). Both authors suggested that the janirids are commensal associates of Limnoria. The harpacticoid copepod Harrietella simulans were observed on the telson, oral appendages, or the legs of the isopod L. lignorum (Vervoort 1950). The copepod most likely attaches itself to the isopod after its metamorphosis into a copepodid. Another association with the wood-excavating species of Limnoria is that with the heterotrich ciliate Mirofolliculina limnoriae, which attaches itself to the dorsal surface of the limnoriid pleotelson (Delgery et al. 2006). This relationship has been characterized as ectoparasitism because the folliculinids are able to feed by intercepting particulates when the limnoriid ventilates its burrow, but the limnoriid’s feeding is suppressed and its swimming is hindered when dispersing (Delgery et al. 2006). Defense of Dwellings Excavating crustaceans are known to display defensive behaviors to defend their burrows and offspring from predators and conspecifics. To physically protect themselves, limnoriids can roll into a ball shape, similar to their terrestrial counterpart, the wood louse (Henderson 1924). To prevent individuals of the same or different species from entering their burrow, excavating crustaceans display several behavioral traits. Males often engage in mate guarding to prevent other males of the same species from copulating with a female (as mentioned in “Heterosexual Pairs”). The

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Fig. 5.8. The amphipod Peramphithoe stypotrupetes and three successive broods in an excavated kelp stipe. From Conlan and Chess (1992) by J.R. Chess.

chelurid T. gomezi was noted to defend its burrow from roving conspecifics by placing the dorsal surface of its heavily calcified quadrate urosome at the entrance of the burrow (Thomas 1979). This defensive posturing was equally successful for both large and small individuals at preventing other individuals from entering the burrow (Thomas 1979). Similarly, limnoriids can use an oval feature, formed by the distal margin of the pleotelson and lateral crests on their segments, to secure the burrow, thus minimizing harsh environmental conditions, including desiccation at low tide (Cookson et al. 2012). Parental care is common among excavating isopods as exhibited in “Sharing of Dwellings.” The aggregation of wood-excavating Limnoria, for example, aids in the defense of their young by enabling a higher concentration of burrows, thus improving water circulation and oxygen supply



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(Fig. 5.6A). The increased circulation allows Limnoria to build their burrows deeper than otherwise possible, with their young farther from potential predators at the burrow entrance (Menzies and Widrig 1955). Sphaeroma quoianum increase the survivorship of their young by having the juveniles remain at the terminal end of the tunnel, in addition to mothers using their pleotelson to block the burrow opening (Davidson 2006). Similarly, female L. chilensis protect their offspring by remaining at the opening of the burrow when cohabiting with their juveniles (Thiel 2003). Although many excavating crustaceans may effectively defend their burrows from intruders, there are examples of other species being able to enter burrows and benefit from conditions within the burrow. Juveniles of S. quadridentatum were observed in burrows of reproductive S. terebrans, with the former benefitting from allomaternal care from the latter. Sphaeroma terebrans apparently were not able to distinguish effectively between their own and foreign offspring, potentially deceived by the small size of the juvenile S. quadridentatum (Thiel 2000). Thiel (2000) postulates that because juveniles of S. terebrans are not highly mobile and remain within the burrow through the parental care period, S. terebrans may not have developed any mechanisms to distinguish their juveniles from others.

TRADE-OFFS FACED BY CRUSTACEANS LIVING IN SELF-CONSTRUCTED DOMICILES The morphological and behavioral adaptations that allow crustaceans to excavate burrows in the substratum provide benefits of shelter, food, and protection, but may involve costs associated with reduced dispersal, damage to chosen habitats, and reduced reproductive output. By understanding these trade-offs, we can better understand the evolution of the excavating lifestyle. The functional morphology of excavating crustaceans is representative of their primary habitat— burrows (see “Morphological Adaptations”). The bulbous head and short, compact body common among these crustaceans (Fig 5.1) may involve costs associated with limited dispersal. The voluminous head, stout body, and short pleopods result in a body shape that is not hydrodynamic, suggesting that these excavating crustaceans are neither fast nor graceful swimmers. Consequently, these crustaceans are not very mobile, with drifting being the main mechanism of dispersal, aided by limited swimming activity. Limnoriids and, in fact, all small crustaceans are most vulnerable when dispersing in the water column (Henderson 2000). Excavating crustaceans are likely to only exit their burrow when necessary to build a new domicile due to a lack of resources or overcrowding. Outside of the burrow, dispersing crustaceans face external threats to their survival (predators or harsh environmental conditions) and, for those species that feed on their host, no access to their food source. Sharing a domicile with a mate, offspring, conspecifics or other species has clear, often symbiotic, benefits (see “Sharing of Dwellings”), but food resources will diminish faster with increased numbers of residents, and there will most likely be greater wear on the burrow. Excavating crustaceans that also feed on their host substrata will damage their burrow at a faster rate, while multiple individuals’ filter feeding will exhaust organic matter faster than an individual would. Increased wear on the burrow will shorten the burrow’s lifetime, forcing the crustacean to migrate sooner. Many crustaceans live in heterosexual pairs to facilitate copulation and mate guarding. Mate guarding protects a male’s investment—the ovigerous female, but is also an energy and time cost, limiting the male from reproducing with other females while guarding. Males are often absent when the offspring are released, possibly due to being expelled by females after copulation because males at the burrow entrance would hamper efficient burrow ventilation. Johnson and Menzies (1956) indicated that males of L. tripunctata are more mobile, either due to extrinsic (expelled by females) or intrinsic factors (actively leaving females’ burrows). Visiting more females’ burrows enables

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone males to copulate with more females but is also associated with increased vulnerability to predators and environmental conditions outside of the protection of a burrow. The life cycle of excavating isopods indicates that they are K-strategists, with small brood sizes and extended parental care (Cragg 2003). An example of L. lignorum has demonstrated that brood sizes may also be density-dependent ( Johnson and Menzies 1956). Stress caused by overcrowding and increased competition for resources may compromise the condition of reproductive females, thereby leading to smaller brood sizes in L. lignorum. Resource limitations are directly related to the area of available wood because the crustacean feeds from its domicile. It was observed that the rate of young being added to the population during overcrowding was half that of the rate of juveniles that were added to an uncrowded population ( Johnson and Menzies 1956). Despite the time cost to the parents, parental care is effective at reducing the effects of predation on juveniles (Thiel 1999b). When the juveniles begin to excavate from within the parental burrow, the juveniles have not yet developed full excavating capacity (Thiel 2003). By enabling their offspring to burrow from within the parental burrow, the parents are allowing the juveniles to bore slowly. Hosting the juveniles for extended time periods in the interior of her burrow may, though, carry substantial costs for the female. The position of the juveniles in the interior of the burrow most likely impedes active burrowing by the female during the maternal care period. This will be particularly relevant for those species that feed on their burrow substratum, such as limnoriid isopods. Juveniles excavating from within the parental burrow may also have direct advantages for the parents, increasing the circulation of water and oxygen in their burrow, but the additional excavating will also structurally weaken the burrow. In general, ventilation of a burrow is necessary for the survival of a crustacean, but it also increases the stress on the substrata.

ECOLOGICAL EFFECTS Burrowing crustaceans impact their hosts and substrata by excavation as well as by feeding. Even though they are rarely longer than a couple of millimeters, these crustaceans can inflict substantial damage due to their sheer numbers, their collective ability to withstand varying environmental conditions, and the potential of rapidly colonizing and forming dense populations in new habitats. Rafting kelp, driftwood, and wooden vessels enable excavating crustaceans to passively disperse across oceans because these various forms of substrata continue to be a source of shelter and food to excavating crustaceans even when in motion (Highsmith 1985, Carlton 1994, Nikula et al. 2010). For example, limnoriid isopods that inhabit kelp holdfasts can be transported over long distances when positively buoyant kelps are detached from the bottom and dispersed with the currents. This process contributes to effective population connectivity and colonization of new habitats (Nikula et al. 2010, Haye et al. 2012). Molecular data provide strong indication that L. stephenseni and P. kidderi, which live in the holdfasts of the large kelp D. antarctica, have colonized the subpolar regions around Antarctica after the last glaciations by rafting on their kelp hosts (Nikula et al. 2010). Dispersal of wood-excavating crustaceans can also occur as a result of driftwood rafting and shipping activities (Svavarsson 1982, Cookson and Cragg 1991, Cragg et al. 1999). Limnoria cristata and L. borealis were reported on beached driftwood in an intertidal mangrove forest and on sunken driftwood in Arctic waters, respectively. Sphaeroma terebrans, for instance, is presumed to have been introduced to the Americas via the Indo-Pacific because it had bored into wooden shipping vessel hulls (Carlton 1994). The passive dispersal of excavating crustaceans introduces non-native species to ecosystems that the crustaceans can adversely impact. Excavating crustaceans can negatively affect their hosts, destroying vital tissue when constructing their burrows. The remaining tissue is more likely to be exposed to microbial infection and



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

also habitation by other species ( Jones 1971). Along 1,000 km of the western Australian coastline, the isopod Limnoria agrostisa damaged up to 20% and 70% of leaf clusters and shoots, respectively, of the seagrass Amphibolis griffithii (Fig. 5.9A; Brearley et al. 2008). Due to the destruction caused to leaf clusters and the malformation of new leaves, the damage may lead to the reduction of the photosynthetic capacity of the shoot (Brearley et al. 2008). In a more extreme case, dense populations of the amphipod P. stypotrupetes together with gastropod grazers can destroy entire kelp beds (Chess 1993). Crustacean borers not only have damaging effects on seagrass and algae, but also can extensively alter coastlines. Sphaeroma quoianum burrows into salt marsh banks, which can expedite sediment loss (Talley et al. 2001). Enclosure experiments have estimated that the marsh edge could recede more than 1 m every year due to S. quoianum infestations (Talley et al. 2001). There are conflicting reports on whether S.  terebrans are positively or negatively impacting mangrove forests. Sphaeroma terebrans excavate burrows into the aerial roots of mangrove trees for shelter (Fig. 5.9B). Simberloff et al. (1978) have claimed that S. terebrans may induce branching of the aerial roots of the red mangrove R. mangle, thus stabilizing the trees from wave action. But it has also been suggested that the death and breakage of the root caused by the burrowing can negatively impact the nutrient provisioning and support system of the entire tree (Brooks and Bell 2001, 2005, Svavarsson et al. 2002). Perry and Brusca (1989), as well as Ellison and Farnsworth (1990), were able to refute the claims of Simberloff et al. (1978) of an increase in lateral branching through

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Fig. 5.9. Damage inflicted by excavating crustaceans. (A) Damage caused to the terminal leaf cluster of the seagrass Amphibolis griffithii by the isopod Limnoria agrostisa; leaf width 6 mm. From Brearley et al. (2008), with permission from Springer. (B) Damage caused by the isopod Sphaeroma terebrans to the aerial roots of the mangrove Rhizophora mangle. From Svavarsson et al. (2002), courtesy of J. Svavarsson. (C) Comparison of undamaged seeds (top) and seeds bored by the tanaid Zeuxo sp. (middle and bottom). From Nakaoka (2002), with permission from Aquatic Botany. (D)  Pinhole disease by boring copepods Amenophia orientalis and Parathalestris infestus in Undaria pinnatifida, scale bar = 1 cm. From Park et al. (2009), with permission from Springer.

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone observations on the activities of other isopods, S. peruvianum and L. clarkae, respectively. These isopods negatively affected the growth rates of the mangrove roots, and, in the latter case, the net root production of burrowed roots was 62% less than that of roots that had not been excavated (Perry and Brusca 1989, Ellison and Farnsworth 1990). Damage to reproductive tissues of the host is likely to have particularly severe impacts on macrophyte fitness. The tanaid crustacean Zeuxo sp. lives in the swathes of the seagrasses Z. marina and Z.  caulescens in Otsuchi Bay in Japan, consuming their seeds by excavating holes into the seeds (Fig. 5.9C). Their burrowing and feeding activities significantly suppress seed production, but although reducing reproductive output, these impacts do not lead to population declines (Nakaoka 2002). The mechanisms of how excavators may impact algal and seagrass blades are not well studied and so can only be speculated. Effects may include reduced transport of nutrients, gases, and photosynthates, which would cause a disruption of growth due to the removal of vascular tissue as a result of burrowing. The burrow itself may impact the epidermis; if the epidermis breaks down, water, fungi, and bacteria may enter; solutes could be lost; or the leaf itself may split (Brearley and Walker 1995). There is also concern of increased ecological damage with increases in seawater temperatures and changes to salinity regimes, resulting in shifts in the geographical range of species (Fig. 5.10). An increase of salinity (and, not as importantly, temperature) in the Tagus estuary promoted the introduction of L. quadripunctata, a major contributor to the destruction of man-made wooden structures in that region (Borges et al. 2010). Figure 5.10 outlines how the feeding rate of L. quadripunctata, determined by its fecal pellet production rate, is impacted by temperature, with the species feeding on wood at a faster rate from 20°C to 25°C (Borges et al. 2009), and also highlights the range of temperatures that different limnoriids inhabit. Davidson and his colleagues (2013) studied the effects of increased seawater temperatures on the burrowing of S. quoianum in polystyrene blocks and found that the isopods excavated the longest burrows in seawater temperatures that were 1.1–5.6°C higher than the temperature of their original habitat. So, increased biological activity 120 Mean fecal pellets per day

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Limnoria borealis Limnoria chilensis Limnoria quadripunctata Limnoria stephenseni Limnoria tripunctata

Fig. 5.10. The relationship between feeding rates (as estimated by fecal pellet production) and water temperature for the isopod Limnoria quadripunctata feeding on wood, redrawn from Borges et al. (2009), with known temperature ranges displayed for other common limnoriids.



Barbara A. Mejaes, Alistair G.B. Poore, and Martin Thiel

on the part of this borer, as well as potentially others, could result in greater damage to their substrata. Also, as we learn more about the problems associated with plastic pollution, borers into polystyrene, such as S. quoianum, could pose an additional source to microplastic pollution: Davidson (2012) estimated that one isopod creates thousands of microplastic particles when excavating a burrow, particles that could in turn harm other fauna.

ECONOMIC EFFECTS Excavating crustaceans also have detrimental economic impacts when excavating into substrata that possess monetary value. Growth of the alga U. pinnatifida, which accounts for 48% of South Korea’s total seaweed production, can be severely impacted by copepod miners (Park et al. 2009). Small holes in the thallus, known as pinhole disease, deem the algae not suitable for human consumption (Fig. 5.9D). This disease is caused by the copepods Amenophia orientalis and Parathalestris infestus and leads to the decay of the thallus (Torii and Yamamoto 1975, Ho and Hong 1988, Park et al. 1990). The disease is prevalent in U. pinnatifida farms in Hokkaido, Japan (Torii and Yammoto 1975), and, in order to minimize economic losses caused by the disease, the algae are harvested earlier than would be otherwise. Economic damage is also caused by the species of Limnoria and Sphaeroma that burrow into wood. These wood-excavating isopods cause significant damage to marine timber, including both ships and piers that are exposed below the water line (Ray 1959, Cragg et al. 1999), and contributing to the annual $1 billion in damage to submerged coastal structures in the United States (Boyle 1988). In New York Harbor, improved water quality in recent years has been associated with an increased abundance of limnorids and related economic challenges with the maintenance of wooden structures (Foderaro 2011). The use of biocides and fumigants or coating timber with wood preservatives to protect these resources from crustacean damage might results in potential toxicological impacts of these measures on the marine environment (Cragg et al. 1999).

FUTURE DIRECTIONS Research needs to be conducted to better understand the behavioral adaptations of excavating crustaceans. Earlier works (Menzies 1954, Henderson and Cragg 1996) have indicated that excavating crustaceans use chemoreception to locate a host, but more research can be carried out to gain better knowledge of how these crustaceans choose their substratum. It is especially difficult to understand the behaviors of crustaceans within burrows because burrows are dark and enclosed. Studying an excavating crustacean’s behavior within its burrow will shed light on how it maintains its domicile and its conspecific and interspecific associations. As we are faced with a changing climate, it will also be important to understand how altered environmental conditions will impact these crustaceans and, in turn, what impact the crustaceans will have on their ecosystems. There are already examples of how the negative impacts of these crustaceans on ecosystems may be increased as a result of increased temperature and altered salinity (see “Ecological Effects”).

CONCLUSIONS Crustaceans that excavate burrows utilize a variety of biotic and abiotic substrata. Despite the different substrata that these crustaceans may favor, they share similar morphological and behavioral

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone adaptations. Strong mouthparts, spheroid heads, and compact bodies aid in excavating and living within their burrows. These morphological adaptations, however, may prove costly when a crustacean is not within its domicile. Excavating crustaceans take advantage of the protective nature of their burrows to mate, reproduce, and care for their offspring. But excavating crustaceans have been documented to have negative impacts on their hosts due to the physical construction of their domiciles and their feeding activities. Their negative impacts can affect natural ecosystems, coastal infrastructure, and economically valuable resources—effects that may be exacerbated by our changing climate.

ACKNOWLEDGMENTS We are very grateful to Simon Cragg for advice and help with the literature and photographs.

REFERENCES Barnard, J.L. 1972. The marine fauna of New Zealand: algae-living littoral Gammaridea (Crustacea, Amphipoda). New Zealand Department of Scientific and Industrial Research Bulletin 210:1–216. Becker, G. 1971. On the biology, physiology and ecology of marine wood-boring crustaceans. Pages 303–326 in E.B.G Jones and S.K. Eltringham, editors. Marine borers, fungi and fouling organisms. OECD, Paris. Boltaña, S., and M. Thiel. 2001. Associations between two species of snapping shrimp, Alpheus inca and Alpheopsis chilensis (Decapoda: Caridea: Alpheidae). Journal of Marine Biological Association of the United Kingdom 81:633–638. Borges, L.M.S., S.M. Cragg, and S. Busch. 2009. A laboratory assay for measuring feeding and mortality of the marine wood borer Limnoria under forced feeding conditions: a basis for a standard test method. International Biodeterioration Biodegradation 63:289–296. Borges, L.M.S., A.A. Valente, P. Palma, and L. Nunes. 2010. Changes in the wood boring community in the Tagus Estuary: a case study. Marine Biodiversity Records 3:1–7. Bousfield, E.L., and P. Marcoux. 2004. The talitroidean amphipod family Najnidae in the north Pacific region: systematic and distributional ecology. Amphipacifica 3:3–44. Boyle, P.J. 1988. Marine wood biodeterioration and wood-boring crustaceans. Pages 167–188 in M.F. Thompson, R. Sarojini, and R. Nagabhushanam, editors. Marine biodeterioration: advanced techniques applicable to the Indian Ocean. Oxford IBH Publishing Co., New Dehli. Brearley, A., and D.I. Walker. 1995. Isopod miners in the leaves of two Western Australian Posidonia species. Aquatic Botany 52:163–181. Brearley, A., G.A. Kendrick, and D.I. Walker. 2008. How does burrowing by the isopod Limnoria agrostisa (Crustacea: Limnoriidae) affect the leaf canopy of the southern Australian seagrass Amphibolis griffithii? Marine Biology 156:65–77. Brooks, R.A., and S.S. Bell. 2001. Colonization of a dynamic substrate: factors influencing recruitment of the wood-boring isopod, Sphaeroma terebrans, onto red mangrove (Rhizophora mangle) prop roots. Oecologia 127:522–532. Brooks, R.A., and S.S. Bell. 2005. The distribution and abundance of Sphaeroma terebrans, a wood-boring isopod of red mangrove (Rhizophora mangle) habitat within Tampa Bay. Bulletin of Marine Science 76:27–46. Carlton, J.T. 1994. Non-indigenous marine and estuarine invertebrates of Florida. Pages 110–118 in D.C. Schmitz and T.C. Brown, editors. An assessment of invasive non-indigenous species in Florida’s public lands. Technical Report Number TSS-94–100. Florida Department of Environmental Protection, Tallahassee, Florida. Cerda, O., I.A. Hinojosa, and M. Thiel. 2010. Nest-building behavior by the amphipod Peramphithoe femorata (Krøyer) on the kelp Macrocystis pyrifera (Linnaeus) C. Agardh from northern-central Chile. The Biological Bulletin 218:248–258.



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Chess, J.R. 1993. Effects of the stipe-boring amphipod Peramphithoe stypotrupetes (Corophioidea: Ampithoidae) and grazing gastropods on the kelp Laminaria setchellii. Journal of Crustacean Biology 13:638–646. Conlan, K.E., and J.R. Chess. 1992. Phylogeny and ecology of a kelp-boring amphipod, Peramphithoe stypotrupetes, new species (Corophioidea: Ampithoidae). Journal of Crustacea Biology 12:410–422. Cookson, L.J. 1990. Australasian species of Limnoriidae (Crustacea: Isopoda). Memoirs of the Museum of Victoria 52:137–262. Cookson, L.J., and J.E. Barnacle. 1987. The performance in Australia after ten years in the sea of single and double preservative treating timber specimens. Material Und Organismen 22:139–160. Cookson, L.J., and S.M. Cragg. 1991. Limnoria cristata (Isopoda: Limnoriidae), a new species of marine wood-borer from Singapore. Raffles Bulletin of Zoology 39:87–97. Cookson, L.J., and M. Lorenti. 2001. A new species of limnoriid seagrass borer (Isopoda) from the Mediterranean. Crustaceana 74:339–346. Cookson, L.J., and D.K. Scown. 1999. Recent marine wood preservation research in Australia. 10th International Congress on Marine Corrosion and Fouling, University of Melbourne: Additional Papers 172–195. Cookson, L.J., S.M. Cragg, and I.W. Hendy. 2012. Wood-boring limnoriids (Crustacea, Isopoda) including a new species from mangrove forests of the Tukang Besi Archipelago, Indonesia. Zootaxa 3248:25–34. Cragg, S.M. 2003. Marine wood boring arthropods: ecology, functional anatomy, and control measures. Pages 272–286 in B. Goodell, D.D. Nicholas, and T.P. Schultz, editors. Wood deterioration and preservation: advances in our changing world. American Chemical Society, Oxford University Press. Cragg, S.M., and G. Daniel. 1992. Chelura terebrans (Crustacea: Amphipoda) is capable of degrading wood independently of its associate, Limnoria. International Research Group on Wood Preservation IRG/WP 4180:1–10. Cragg, S.M., and C.R. Levy. 1979. Attack by the crustacean Sphaeroma on CCA-treated softwood in Papua New Guinean waters. International Journal of Wood Preservation 1:161–168. Cragg, S.M., A.J. Pitman, and S.M. Henderson. 1999. Developments in the understanding of the biology of marine wood boring crustaceans and in methods of controlling them. International Biodeterioration & Biodegradation 43:197–205. Davidson, T.M. 2006. The invasion of the Australiasian burrowing isopod (Sphaeroma quoianum) in Coos Bay, Oregon. Thesis, Department of Biology, Graduate School of the University of Oregon. Davidson, T.M. 2012. Boring crustaceans damage polystyrene floats under docks polluting marine waters with microplastic. Marine Pollution Bulletin 64:1821–1828. Davidson, T.M., S.S. Rumrill, and A.L. Shanks. 2008. Colonization and substratum preference of an introduced burrowing crustacean in a temperate estuary. Journal of Experimental Marine Biology and Ecology 354:144–149. Davidson, T.M., C.E. de Rivera, and J.T. Carlton. 2013. Small increases in temperature exacerbate the erosive effects of a non-native burrowing crustacean. Journal of Experimental Marine Biology and Ecology 446:115–121. Delgery, C.C., S.M. Cragg, S. Busch, and E.A. Morgan. 2006. Effects of the epibiotic heterotrich ciliate Mirofolliculina limnoriae and of moulting on faecal pellet production by the wood-boring isopods, Limnoria tripunctata and Limnoria quadripunctata. Journal of Experimental Marine Biology and Ecology 334:165–173. Ellison, A.M., and E.J. Farnsworth. 1990. The ecology of Belizean mangrove-root communities. I. Epibenthic fauna are barriers to isopod attack of red mangrove roots. Journal of Experimental Marine Biology and Ecology 142:91–104. Foderaro, L.W. Cleaner harbor has a downside: pests that plague park construction. The New York Times. August 23, 2011. Gambi, M.C., B.I. van Tussenbroek, and A. Brearley. 2003. Mesofaunal borers in seagrasses: world-wide occurrence and a new record of boring polychaetes in the Mexican Caribbean. Aquatic Botany 76:65–77. Gambi, M.C., B. Trani, and M.C. Buia. 2005. Taxonomic diversity and distribution of polychaete and isopod borers on the sheaths of the seagrass Posidonia oceanica: analysis at regional scale along the coast off Sardinia (Italy). Italian Journal of Zoology 72:141–151.

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Crustaceans Inhabiting Domiciles Excavated from Macrophytes and Stone Gestoso, I., C. Olabarria, and J.S. Troncoso. 2014. Selection of habitat by a marine amphipod. Marine Ecology. 35:103–110. Harding, J.P. 1954. The copepod Thalestris rhodymeniae (Brady) and its nauplius, parasitic in the seaweed Rhodymenia palmata (L.) Grev. Proceedings of the Zoological Society of London 124:153–161. Haye, P.A., A.I. Varela, and M. Thiel. 2012. Genetic signatures of rafting dispersal in algal-dwelling brooders Limnoria spp. (Isopoda) along the SE Pacific (Chile). Marine Ecology Progress Series 455:111–122. Henderson, J.T. 1924. The gribble: a study of the distribution factors and life-history of Limnoria lignorum at St. Andrews, N.B. Contributions to Canadian Biology. 2:309–325. Henderson, S.M. 2000. The swimming behavior of the marine wood borer Limnoria quadripunctata (Isopoda: Limnoriidae). Crustacean Issues 12:227–238. Henderson, S.M., and S.M. Cragg. 1996. The role of contact chemoreception in location of wood by the marine borer Limnoria: Isopoda. International Research Group on Wood Preservation IRG/WP 96:1–11. Henderson, S.M., S.M. Cragg, and A.J. Pitman. 1995. Wood detection by the marine isopod Limnoria. International Research Group on Wood Preservation IRG/WP 95:1–14. Hicks, G.R.F., and J. Grahame. 1979. Mucus production and its role in the feeding behavior of Diarthrodes nobilis (Copepoda: Harpacticoida). Journal of Marine Biological Association of the United Kingdom 59:321–330. Highsmith, R.C. 1985. Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Marine Ecology Progress Series 25:169–179. Ho, J.S., and J.S. Hong. 1988. Harpacticoid copepods (Thalestridae) infesting the cultivated Wakame (brown alga, Undaria pinnatifida) in Korea. Journal of Natural History 22:1623–1637. Ishimaru, S. 1996. Taxonomic review of the family Biancolinidae (Amphipoda: Gammaridea), with description of a new species from Japan. Journal of Crustacean Biology 16:395–405. Johnson, M.W., and R.J. Menzies. 1956. The migratory habits of the marine gribble Limnoria tripunctata Menzies in San Diego Harbor, California. Biological Bulletin 110:54–68. Johnson, W.S., M. Stevens, and L. Watling. 2001. Reproduction and development of marine peracaridans. Advances in Marine Biology 39:105–260. Jones, L.G. 1971. Studies on selected small herbivorous invertebrates inhabiting Macrocystis canopies and holdfasts in southern California help beds. Beiheft zur Nova Hedwigia 32:343–367. Karplus, I. 1987. The association between gobiid fishes and burrowing alpheid shrimps. Oceanography Marine Biology: An Annual Review 25:507–562. Kern, M., J.E. McGeehan, S.D. Streeter, R.N.A. Martin, K. Besser, L. Elias, W. Eborall, G.P. Malyon, C.M. Payne, M.E. Himmel, K. Schnorr, G.T. Beckham, S.M. Cragg, N.C. Bruce, and S.J. McQueen-Mason. Structural characterization of a unique marine animal family 7 cellobiohydrolase suggests a mechanism of cellulose salt tolerance. Proceedings of the National Academy of Sciences 110:10189–10194. King, A.J., S.M. Cragg, Y. Li, J. Dymond, M.J. Guille, D.J. Bowles, N.C. Bruce, I.A. Graham, and S.J. McQueen-Mason. 2010. Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes. Proceedings of the National Academy of Sciences USA 107:5345–5350. Kühne, H., and G. Becker. 1964. Der Holz-flohkrebs Chelura terebrans Philippi (Amphipoda, Cheluridae). Beihefte der Zeitschrift fur angewandte Zoologie 1:1–141. Kussakin, O.G., and M.V. Malyutina. 1989. A new species of deep-sea marine borer of the family Limnoriidae (Isopoda, Flabellifera) from the Okhotsk Sea. Crustaceana 56:8–13. Lörz, A.N., N.M. Kilgallen, and M. Thiel. 2010. Algal-dwelling Eophliantidae (Amphipoda): description of a new species and key to the world species, with notes on their biogeography. Journal of the Marine Biological Association of the United Kingdom 90:1055–1063. Lowry, J.K. 1974. A new species of the amphipod Biancolina from the Sargasso Sea. Transactions of the American Microscopical Society 93:71–78. Loyola e Silva, J.D. 1960. Sphaeromatidae do litoral Brasileiro (Isopoda-Crustacea). Boletim Da Universidade Do Parana, Zoologica 4:1–182. Menzies, R.J. 1951. A new genus and new species of asellote isopod, Caecijaera horvathi, from Los Angeles-Long Beach Harbor. American Museum Novitates 1542:1–7. Menzies, R.J. 1954. The comparative biology of reproduction in the wood-boring isopod crustacean Limnoria. Bulletin of the Museum of Comparative Zoology at Harvard College 112:363–388.



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6 CRUSTACEANS IN MOBILE HOMES

Patsy A. McLaughlin

The author, Patsy A. McLaughlin, passed away during the editing process for this book. Revisions for this chapter were carried out posthumously by Rafael Lemaitre, Martin Thiel, and Lucas Eastman.

Abstract Hermit crabs depend on mobile homes to protect their vulnerable pleons. This chapter examines the diversity of such homes, specifically shells obtained from dead organisms, including gastropods, scaphopods, bivalves, and pteropods. Some crustaceans seek mobile homes in the form of symbiotic housing, taking advantage of diverse relationships with other phyla including Porifera, Cnidaria, Bryozoa, and Polychaeta. These symbiotic relationships can permit the hermit crab to grow without leaving its original shell, whereas in other instances the symbionts act as a living shell for the hermit crab. There also exist some important alternatives to symbiotic and conventional shell housing—certain crustaceans have utilized xylicolous (wood) and petricolous (stone) dwellings, which provide a seemingly clumsy and unorthodox but effective shelter from predators. Certain members of Tanaidacea and Amphipoda are highlighted because they are not hermit crabs but also use mobile homes. Both these crustaceans and hermit crabs have developed morphological specializations that make them well-adapted to mobile home living.

INTRODUCTION Although many invertebrates utilize exogenous shelters, the vast majority of hermit crabs remain mobile with their shelters, which are herein termed carcinoecia (“house of crustacean”). This concept of a combination of mobility and protection instantly invokes an image of a snail shell-dwelling crab, and certainly a great number are to be found in that category. But hermit crabs are not restricted

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Crustaceans in Mobile Homes in their housing preferences to dextral gastropod shells, nor are hermit crabs the only crustaceans that take advantage of mobile homes. In this chapter, we review the array of mobile homes available to crustaceans and the morphological specializations of their occupants. Mobile homes are interpreted here as places where the crustaceans abode rather than associations in which one component simply provides camouflage for the other, such as the relationships between dromiid crabs and their sponges.

HISTORICAL PERSPECTIVE OF HERMIT CRAB SHELLS Hermit crabs are most commonly associated with cochlean carcinoecia, but just as there is vast morphological diversity within this anomuran superfamily (Paguroidea; sensu McLaughlin et al. 2007), so is there appreciable diversity in their choice of protection. The documented association between hermit crabs and gastropod shells dates back to Aristotle in the fourth century B.C., although apparently it was his belief that both crab and shell were generated spontaneously from mud and sand. Eighteenth-century studies led researchers to suggest that the animals secreted their own shells; however, by the nineteenth century, carcinologists had observed that many familiar hermit crabs had soft, asymmetric, twisted pleons that they protected by inserting them into gastropod shells. Thus, it is not surprising that pleonal asymmetry became accepted as the ancestral condition of paguroids (Richter and Scholtz 1994). The pleonal symmetry observed in most pylochelids was acknowledged as setting that family apart from other paguroids. Nevertheless, their symmetry was believed to have been secondarily acquired, seemingly supported by evidence from the fossil record, even though only a few fossils unequivocally confirmed gastropod/paguroid associations, and in none could the pleons be reconstructed. However, a highly significant recent fossil discovery indicated that the precursor to gastropod housing might well have been ammonite cephalopods. Fraaije (2003) described a perfectly preserved heterochelous Early Cretaceous hermit crab protruding from such an ammonite shell. He suggested that the continuous use of such shells by succeeding generations of hermit crabs might provide an overlooked biological explanation for the occurrence of ammonite shells after their presumed demise above the Cretaceous-Tertiary extinction interval. This fossil might also indicate that early hermit crabs possessed generally straight, symmetrical pleons adapted for use with planispiral ammonite shells and that pleonal twisting and asymmetry evolved with the transition of hermit crabs to the stronger and more easily transported conispiral gastropod shells. Even more recently, van Bakel et al. (2008) identified the first fossil hermit crab carapaces, these belonging presumably to members of the Pylochelidae, Diogenidae, and Parapaguridae, and all from strata of Late Jurassic age. These authors suggested that “from a symmetrical ancestor similar to a pylochelid or even pylochelids proper, other paguroid families evolved by adapting to different kinds of shelters. Loss of calcified pleonal segments, reduction or adaptation of posterior pereopods, decalcification of the posterior carapace and asymmetry (McLaughlin 2003) subsequently evolved from the Early Jurassic onward” (p.137). The fossil record offers no substantive information as to whether the transition from ammonite to gastropod shell was followed subsequently by reversion of some paguroids to nonspiral domiciles or whether two parallel but distinct ecological pathways evolved simultaneously. Whatever the choice of shelter might have been for the early paguroid, adoption of mollusk shells for mobile housing not only could have enormously extended the ecological life span of the average snail shell (Vermeij 1977), it also unquestionably permitted typical hermit crab colonization from the intertidal to abyssal depths throughout most of the world’s oceans.



Patsy A. McLaughlin

MOLLUSKAN HOUSING Gastropod Shells By far the most frequently utilized mollusk shells are of dextrally coiling gastropods, and most recent paguroid taxa are admirably adapted to these carcinoecia. These adaptations include (i) reduced fourth pereopods that, like the fifth, typically are carried within the shell and, with the aid of pereopodal rasps, assist in shell stability; (ii) the membranous pleon that, while providing flexibility and torsion, also allows the crab muscular and hydrostatic control over shell positioning (Chapple 1973); (iii) reduction and/or loss of most pleonal appendages on the right side of the pleon, the side most closely adjacent to the wall of the shell; (iv) asymmetric development; and (v) specialization of the uropods, which together with the reduced and modified telson, provide a form of holdfast to aid in allowing the animal to maintain a grasp on its shell. How do hermit crabs obtain these shells? Hermit crabs typically utilize shells of dead gastropods that can be obtained either by locating an empty shell or obtaining it from another crab. Hermit crabs in need of a new home are attracted to dead gastropods via chemical cues (Rittschof 1980). Fig. 6.1 provides a photographic account of a species of Dardanus exploring, and ultimately accepting, a new home, which can be briefly summarized as follows. When a crab in search of a

Fig. 6.1. A specimen of Dardanus sp. acquiring a new shell. Photos by D. Bartlett, courtesy of A.J. Provenzano. (A) In search of a new home. (B) A likely potential. (C–F) Investigating the new shell. (G–I) Moving in.

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Crustaceans in Mobile Homes housing upgrade (Fig. 6.1A) sights a new potential home, it makes initial contact with the “new” shell with its antenna, a walking leg, or chela (Fig. 6.1B). The crab grasps the shell and explores the surface with its chelipeds and walking legs, first externally and then internally (Fig. 6.1C,D,E). If the crab finds this new shell satisfactory, it releases its pleonal grip on the old shell and quickly swings its pleon into the new shell (Fig. 6.1F,G,H), leaving the old shell for another crab in need. As is often the case in nature, the crab may similarly reinvestigate the shell it has just abandoned and may elect to return to its old dwelling or move on with its new acquisition. Decisions of acceptance or rejection are particularly influenced by size, weight, overall condition, and aperture shape of the shell (e.g., Lizka and Underwood 1990, Tricarico and Gherardi 2006). But sometimes color (Partridge 1980), shell specificity (Hazlett 1989), and the presence or absence of epibionts (Mercando and Lytle 1980, Brooks and Mariscal 1985) also influence the decision. Obtaining a shell from another hermit crab is more difficult and often involves complex agonistic behavior referred to as “shell fighting.” In its most simplistic form, as reported by Hazlett and Bossert (1965) and Elwood and Neil (1992), at the onset of a fight the attacker (usually the larger of the two crabs) executes some form of chela display to which the defender responds by withdrawing into its shell (Gherardi and Tricarico 2011). With the defender tightly withdrawn, the attacker grasps the margins of the defender’s shell and proceeds to examine the shell with one of its walking legs and/or chelipeds, first externally and then the aperture internally. During the attacker’s exploration, it may also gently rock the defender’s shell a few times. Once the exploration is complete, the rocking is replaced by much more vigorous rapping (Briffa and Elwood 2002). The attacker holds the defender’s shell firmly with its walking legs and hits its shell against the defender’s or forcefully pulls the defender’s shell to its own. It is not uncommon during the attack for the attacker to grasp one or more of the defender’s appendages and forcefully attempt to evict it from its shell. The fight continues until the defender is evicted, signals surrender, or the attacker tires of the fight and releases the defender. To indicate surrender, the defender rapidly taps the attacker’s chelipeds with its own walking legs, then releases its pleonal grip on its shell and allows itself to be extradited from its shell. The victor may continue to hold the defeated crab while exploring its newly won shell or may release the naked crab. But it is only after the victor has chosen whether to move into the new shell or retain its old one that the defeated crab is free to move into the rejected shell. When shell resources are limited, as they frequently are in shallow-water environments (Hazlett 1983, Scully 1983), most hermit crabs will resort to any substitute available to protect their vulnerable pleons (Ďuriš 1992). However, numerous studies have shown that when adequate shell supplies are available, some hermit crabs will utilize shells of several different gastropod species (shell generalists), whereas others are quite specific in their shell choices (shell specialists; Hazlett 1989, Vafeiadou et al. 2012). For example, Hazlett (1989) found that Clibanarius zebra in Hawaii occupied shells of Trochus, Drupella, Nassarius, and Nerita, whereas the sympatric Calcinus seurati was found almost exclusively in shells of Nerita. In addition to the problems of shell availability, the shell shape, weight, and quality have been shown to greatly affect crab survivorship, reproduction, and growth (Elwood and Neil 1992, Benvenuto and Gherardi 2001). Particular shell shapes and sizes also influence certain crab morphological attributes as well. The use of narrow-aperture shells of Conidae and Olividae is thought to be correlated with the flattened cephalothorax seen in species of Ciliopagurus and Clibanarius eurysternus, whereas pleonal reduction appears to be influenced by the use of small-sized shells, as in certain species of Catapagurus. However, choice of housing is not always a “family affair.” As was demonstrated by Rodrigues et  al. (2000) for Calcinus verrillii, a species endemic to Bermuda, the carcinoecia of choice for females were immobile vermetid and turritellid tubes, whereas males of that species occupied mobile gastropod shells of the genus Cerithium. Gherardi (2004) found a similar sexual preference in the Mediterranean Calcinus tubularis. Females exclusively occupied vermetid tubes, whereas males utilized gastropod shells of several species as availability permitted.



Patsy A. McLaughlin

Despite the obvious advantages afforded to hermit crabs by their gastropod shells, there are disadvantages as well. Two in particular—shell availability and crab growth—may have been instrumental in producing modifications to existing resources or adaptations to alternative carcinoecia. Most marine gastropods produce dextrally spiraled shells; however, there are a few aberrant sinistral species among them, and only one family (Triphoridae) of almost exclusively sinistral members. As previously noted, empty dextral shells of faultless or even good quality frequently are in short supply, and although there are far fewer gastropods with shells that spiral sinistrally, it would appear that hermit crabs “in need” can at least temporarily occupy these, and some even prefer them. Hazlett and Herrnkind (1980) indicated that Clibanarius vittatus in Florida frequently inhabited the sinistral Busycon contrarium. Kosuge and Imafuku (1997) found not only C. vittatus in a B. contrarium shell, but specimens of Diogenes pallescens (as Diogenes gardineri) in shells of Mastonia rubra and Calcinus latens in a shell of Cautor levukensis. In the laboratory, Imafuku (1994) was able to induce crabs that occupied inadequate dextral shells to accept sinistral shells of Antiplanes contraria. Imafuku observed that crabs encountering dextral shells always rotated the shells to the left to remove any debris before entering, whereas crabs coming in contact with sinistral shells tended to rotate the shells to the right, but their behavior patterns were not consistent. Although a variety of gastropod mollusks provide mobile homes for the majority of hermit crabs (Fig. 6.2A–F), some have found shells of scaphopod (Fig. 6.2G), bivalve (Fig. 6.2H,I,J), and pteropod (Fig. 6.2K) mollusks preferable. Scaphopod Shells The number of hermit crabs that occupy scaphopod (tusk) shells is relatively small when measured against their gastropod-dwelling relatives; nonetheless, the former kind of shells are the domiciles of choice for some members of five of the six families, and all reflect this preference in their pleonal morphology. As might be expected, the pleons of scaphopod-dwelling hermit crabs are straight rather than exhibiting any degree of torsion, the uropods are symmetrical or nearly so, and at least the right chela frequently is operculate. Members of the Pylochelidae, the so-called “symmetrical hermit crabs” of Forest (1987a), with their elongate and segmented pleons would appear the best suited for tusk shell occupation, and species of a few genera do utilize these shells. Among “asymmetrical” hermits whose pleons typically exhibit at least some degree of torsion, straightening of the pleon suggests a certain amount of pleonal plasticity. In the laboratory, Imafuku and Ando (1999) were able to observe 47 specimens of Pagurus imafukui, one of the few species of the genus that routinely occupies tusk shells. Although when “naked,” the crabs curled their pleons to the right, they had no difficulties inserting these into the straight-sided tusk shells available. The authors found that when given a choice between a dextral gastropod shell and a scaphopod shell, the majority of these crabs chose the latter. This result supports the hypothesis that the selection of scaphopod shells may be a matter of choice, not necessity, because of a limited supply of dextral shells. Although tusk shell occupancy does not appear to be obligatory for most taxa, in species of Pylopagurus, the alternative to the scaphopod carcinoecium usually is a vermetid or worm tube. The few specimens known of the family Pylojacquesidae have been found exclusively in tusk shells. Bivalve Shells Adoption of halves of bivalve shells as carcinoecia by hermit crabs requires greater morphological adaptations than that seen in either gastropod or tusk dwellers, which may explain why their use has been more limited. Despite their familial differences, the monotypic parapagurid Bivalvopagurus shares certain characters with the few pagurid genera known to occupy the bivalve shell habitat. These include moderate to well calcified cephalothoraxes; reduced, but rather bulbous pleons;

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Fig. 6.2. Examples of molluskan mobile homes utilized by hermit crabs: (A–F) Gastropods. (G) Scaphopod. (H–J) Bivalves. (K) Pteropod. A, G, H, J, courtesy of T.-Y. Chan; B, C, E, courtesy of G. Paulay; F, I, courtesy of A.J. Provenzano, Jr.; D, courtesy of A.J. Kohn; and K, from McLaughlin and Rahayu (2006), with permission from Zootaxa.

and symmetrical uropods. However, unlike the pagurid bivalve users, the pleon of B.  sinensis is only partially protected by the clam shell. The shelter is expanded by an actinian attached to the shell whose mantle surrounds and extends the margins of the shell (Lemaitre 1993). Of the five pagurid genera of bivalve users, Alainopagurus, Alainopaguroides, Porcellanopagurus, Patagurus, and Solitariopagurus, all are notable in having entirely lost male pleopods and reduced the number of female pleopods to three (McLaughlin 2000a, Anker and Paulay 2013). However, only in species of Porcellanopagurus and Solitariopagurus are the females’ eggs carried dorsally and entirely covered by the bivalves. Only limited observations have been made on the means by which bivalve-dwelling hermit crabs secure their coverings. McLaughlin (2000a) reported that, in New Zealand, Porcellanopagurus filholi had been found with their telsons and uropodal endopods lodged securely in the umbos of their shells. In contrast, McLaughlin (personal observation) found that specimens of this same species from Japan utilized numerous bivalve shells that lacked well-developed umbos. It appeared that it was a combination of telson, spatulate rami of the uropods, and the posterior



Patsy A. McLaughlin

fleshy portions of the pleons that held these shells in place. The unusual condition of pleon-telson separation found in some but not all species of Porcellanopagurus and Solitariopagurus (McLaughlin 2000a,b) was discussed by Ko and McLaughlin (2008) in relation to “shell carrying” by species of Porcellanopagurus, with specific emphasis on P. nihonkaiensis. According to these authors, the membranous integument of the displaced telson makes it unlikely that the telson is involved at all in shell carriage. Instead, the authors suggested that the bivalve shells were held in place through the use of the uropodal rasps in combination with the hydrostatic pressure of the pleons and perhaps aided by the hooked dactyls of the fourth pereopods. Pteropod Shells McLaughlin and Rahayu (2006) described the hermit crab genus Pteropagurus as containing two species of hermit crabs that appeared uniquely adapted to pteropod mollusk shells. However, they were unaware that, in the western Atlantic, the cnidarian Adamsia sociabilis settles initially on small shells occupied by young crabs of Catapagurus sharreri and are always carried about by these hermit crabs. The nuclei of the carcinoecia are fragments of pteropod shells or worm tubes that frequently are reabsorbed by the cnidarian. It is probable that reabsorption was the reason pteropod shells were not, until McLaughlin and Rahayu’s (2006) discovery, recognized as viable carcinoecia of hermit crabs. Adaptations by these hermit crabs to the shells included reduced and somewhat swollen but straight pleons and carriage of the uropods and telson, which were folded beneath the pleon. These modifications appeared very well suited to the smooth, straight-sided shells of the pteropod genus Cuvierinia. That species of Pteropagurus are shell specialists was demonstrated by McLaughlin and Rahayu (2008) who found that even when empty shells of a second pteropod species were available, hermit crabs of at least two of the three known Pteropagurus species utilized only shells of Cuvierinia columnella. However, these authors also found that the second pteropod species was utilized by a sympatric species of the genus Catapagurus, albeit not exhibiting similar adaptive morphology.

SYMBIOTIC HOUSING The increase in body size that usually accompanies each successive molt requires that the hermit crab periodically search for a larger shell or find a means to increase the size of its existing carcinoecium. Clearly, the hermit crab cannot increase the physical size of its cochlean or other molluskan abode, but it can, and often does, enlist the aid of epifaunal symbionts to do that for it or provide an alternative. Members of three invertebrate phyla in particular—Porifera, Cnidaria, and Bryozoa— play major roles in these symbiotic relationships, but most are facultative associations rather than obligate (sensu Williams and McDermott 2004). Porifera The association of hermit crabs with sponge-covered gastropod shells has been reported for more than a century (Williams and McDermott 2004), with the most common sponges belonging to the family Suberitidae. But, surprisingly, despite their commonality, these associations have received little detailed study. Wells (1969, as Xestospongia halichondrioides) and Sandford and Brown (1997) have described the interaction between a hermit crab and its sponge associate, Spongosorites suberitoides (Fig. 6.3A) as the relationship progresses. This sponge has an inner chamber, initially contiguous with the shell aperture, which leads to an external opening that is shaped and maintained by the hermit crab. As the sponge grows, further embedding the shell, the hermit crab leaves the shell, maintaining

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K Fig. 6.3. Home “building helpers.” (A, B) Sponges. (C–I) Various cnidarians. ( J, K) Bryozoans. (L)  Polychaete. A, courtesy of F. Sandford; B, D, L, courtesy of T.-Y. Chan; C, I, by T.-Y. Chan, courtesy of R. Lemaitre; E, by J. Shoup, courtesy of A.J. Provenzano, Jr.; F, by M.R. Gilligan, courtesy of A.J. Provenzano, Jr.; G, H, courtesy of R. Lemaitre; J, courtesy of C. McLay; K, courtesy of D.L. Felder.

bodily contact only with the inner spirally configured sponge chamber and the external opening. These authors found no evidence that the embedded shells were eroded by the sponge; however, Hart (1971) and van Soest (1993) apparently found that, in later growth stages, the shells were completely dissolved by the sponge. There also is disagreement on whether the sponge actually enlarges the hermit’s living quarters. Hart (1971) reported that the cavity of the sponge symbiont of Pagurus stevensae in the Pacific Northwest increased in size with growth of its crab. In contrast, Sandford (2003) found no evidence to suggest that sponge shelters were utilized for long-term occupancy by Pagurus impressus in Florida. In fact, his data indicated that sponges provided only suboptimal conditions, and their extensive use might be attributed to competition by more aggressive species or scarcity of appropriate “clean” shells. Carcinoecia of the diogenid genus Cancellus most commonly are cavities in pumice rock, but one species, C. spongicola, as its name suggests, most often utilizes siliceous sponges (Mayo 1973), apparently as a matter of preference. Whether by choice or “last resort,” an occasional pylochelid has been captured in a rather ill-fitting sponge (Fig. 6.3B), but it is probable that these latter observations represent incidental associations rather than typical home choices.



Patsy A. McLaughlin

Cnidaria One of the frequently quoted “classical” examples of a symbiotic relationship is the association between the hermit crab Pagurus bernhardus and the colonial hydroid Hydractinia echinata. Although it was speculated that the hydractinian continuously enlarged the hermit’s “house” by building on the lip of the shell and guarded the entrance with a fringe of special spiralzoids, this has not been experimentally proven. In fact, much of the available evidence suggests that it is the hydroid that benefits most from the association (Williams and McDermott 2004 and references therein). For example, hydroids can have negative effects on the reproductive potential of hermit crabs (Damiani 2003). Schijfsma (1935) conducted a series of experiments to address the question of the preference by P. bernhardus for “clean” shells or those with a covering of Hydractinia. She concluded that whereas P. bernhardus eventually settled into shells covered by H. echinata in 41 out of 66 cases, it could not be said with confidence that this hermit crab had a predilection for shells covered with the cnidarian. Sandford (2003) reported that Floridian populations of Pagurus pollicaris showed a significant association with a species of Hydractinia, whereas sympatric populations of P. impressus did not. In the Pacific Northwest, Labidochirus splendescens is found almost exclusively in small gastropod shells covered by hydractinians, but whether the association is mutually beneficial has not been investigated. Although only the pleon of L. splendescens is covered by the shell, the well-calcified carapace of the crab appears to preclude the need for protection by the hydractinian. It is evident that some species of hermit crabs exhibit a preference for shells harboring a colony of Hydractinia, whereas others entirely avoid similar shells. Species of Hydractinia are not the only colonial hydroids associated with hermit crabs; however, the relationships of the genera Hydrocorella, Janaria, and Polyhydra all appear to be obligate (Williams and McDermott 2004). These hydroids also differ from Hydractinia in developing calcified exoskeletons. Although Polyhydra is said to differ from Hydractinia only in the calcification of the exoskeleton, Hydrocorella and Janaria develop distinctive branches from the surfaces of the shells they cover. Although all provide mobile shelters for certain hermit crabs, perhaps the most frequently recognized is Janaria mirabilis, commonly known as a staghorn (Fig. 6.3F), which is home to several species of the hermit crab genus Manucomplanus. Despite the awkwardness of such carcinoecia, Smith (1969) found that a hermit could carry a home nearly 30 times its own weight. Numerous sea anemones are facultative or obligate associates on the gastropod, bivalve, scaphopod, or pteropod shells sheltering hermit crabs and some, through their own growth, allow the crabs to avoid switching shells (Ross 1974). But only a few actually provide the carcinoecia themselves, such as species of the genera Adamsia, Epizoanthus, and Stylobates. Adamsia obvolva, which is an obligate associate of Sympagurus pictus (Fig. 6.3C), wraps its pedal disc around the gastropod shell in which the hermit crab lives and secretes a thin, chitinous carcinoecium that lies between the pedal disc ectoderm and the shell surface. The carcinoecium also may extend beyond the lip of the underlying shell, enlarging the living chamber of the hermit crab (Daly et al. 2004). Although some zoanthids settle directly on their hermit crab hosts, the majority also begin with settlement on the hermit’s shell. After attaching to the shell, the zoanthid develops polyps that grow to encompass the shell entirely. The growth of the zoanthid conforms to contours of the shell or may even replace it. Again, as a result, the crab does not have to change housing with its own growth. Paguropsis typica “wears” a species of the Epizoanthus, E. paguriphilus, much like a sack (Fig. 6.3D), which it apparently is capable of pulling up around its body with its chelate fourth pereopods. Munidopagurus macrocheles evidently also never uses a shell. It “wears” its unidentified anemone, which attaches on the crab’s telson and expands its mantel to encompass the crab’s pleon (Fig. 6.3E) much like a “backpack.” In this species, both the uropods and fourth pereopods are modified to hold the anemone in place and stretch it over the pleon (Provenzano 1971). Several other species of Epizoanthus also form associations with a number of hermit crabs, particularly with those of the family Parapaguridae (Fig. 6.3G,H,I). Although most are facultative relationships, a few are obligate, similar to those of

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Crustaceans in Mobile Homes Parapagurus spp. (Lemaitre 1999), M. macrocheles, and P. typica. Development in Stylobates is quite different from that of Epizoanthus or Adamsia in that, following settlement on the shell, the anemone secretes a chitinous covering that grows in the form of a coiled shell (Fautin Dunn et al. 1981); although described as a gastropod in 1903, it was recognized several years later as actually being an anemone. Interestingly, among these obligate associations, Sympagurus villosus is usually found housed only in colonies of a species of Epizoanthus, whereas the closely related Sympagurus dofleini usually occupies the “false shell” of Stylobates aeneus (Lemaitre 2004). Bryozoa The associations between bryozoans and hermit crabs date back as far as the mid-Jurassic, although it is the distinctive form of the bryozoan colony rather than the presence of fossilized crabs that frequently has been documented (Taylor 1991). Once settled on a crab’s shell, the bryozoan produces a colony of one of two types that encrusts the entire shell. In one instance, the colony grows by budding new layers of zooids above the basal layer, resulting in a rounded covering of the shell. In the second, the colony grows outward from the region of the shell aperture to form a helicospiral tube (Taylor et al. 1989). This growth may also be of two types: tightly wound spirals (involuted) or loosely wound and separated from the body of the colony (evoluted). Taylor et al. (1989) found that the helicospiral growth of the bryozoan’s colony was the result of the activities and growth of the hermit crab (Fig. 6.3J), with the bryozoan colony increasing its tube length and diameter to accommodate the hermit’s increase in size. When the hermit crab has outgrown its original gastropod housing, it abandons it at the rear of the tube and lives exclusively within the cavity formed by the bryozoan. Taylor et al. (1989) noted that hermit crabs occupying carcinoecia consisting of bryozoan colonies rarely changed domiciles or engaged in shell fights. Darrell and Taylor (1989) reported that hermit crabs were capable of mobility in bryozoan housings nearly 100 times greater than the tenant’s own weight. One tube-building bryozoan, Hippoporidra calcarea, looks remarkably like the hydractinian J. mirabilis. However, whereas the hydractinian colony produces several branches, H. calcarea usually develops only a pair of branches from its spiral axis (Fig. 6.3K), which may account for its common name the “Texas longhorn” (Smith 1969). Polychaeta Tube-building polychaete worms, particularly of the family Sabellariidae, form extensive reef-like bioherms inhabited by a variety of crustaceans; however, these provide only sessile housing. Two species of the pagurid genus Discorsopagurus, D. maclaughlinae, and D. tubicola, are routinely found in detached polychaete tubes (Komai 2003) permitting them the same freedom of movement that is provided by other alternative carcinoecia. In contrast, another species of the genus D. cavicola appears to have voluntarily selected a sessile lifestyle. It has been found only in boreholes in clay and hard rock (Komai 2003). Interesting, Gherardi (1996) found that in its natural habitat, the homes of D. schmitti were always attached tubes of Sabellaria cementarium. However, when provided with a choice in the laboratory, this species would more frequently select free tubes or even gastropod shells. Her results suggest that although the crabs prefer mobility, resource limitations have forced this species to adapt to a sedentary lifestyle.

ALTERNATIVES TO SYMBIOTIC HOUSING In addition to the symbiotic relationships that enable numerous hermits either to enhance their molluskan carcinoecia or replace them, some have found unorthodox solutions to the housing problem. Of these, the most common are xylicolous (wood) and petricolous (stone) dwellings.



Patsy A. McLaughlin

Until recently, virtually all of these alternatives were thought to restrict their hermit crab occupants to sessile lives unless they ventured out, without protection, for food or reproductive purposes. However, field and laboratory observations have shown that hermit crabs are as capable of moving about with their awkward and clumsy abodes in place just as they are with cochlean homes. Xylicolous Dwellings Numerous species of “symmetrical” pylochelids select cavities, often excavated by wood-boring organisms, in pieces of hollow-stemmed plants such as bamboo or submerged rotting wood (Fig. 6.4C–G) for their carcinoecia. The walls apparently are smoothed by the occupant, often using the rasps of tubercles on the carpi of the chelipeds and enlarged by similar actions as the animal grows (Forest 1987a,b). The pagurid genus Xylopagurus similarly inhabits hollows in bamboo or rotting wood (Fig. 6.4A,B), but the similarity ends there. The cavities occupied by pylochelid species are open only at one end, and the animals insert their pleons into the hollows first. The xylopagurid dwelling is open at both ends, and the animal enters head first. The posterior opening is securely closed by the crab’s opercular-shaped sixth pleonal tergite (Lemaitre 1995). Petricolous Dwellings Inhabitants of soft stone shelters also occupy deeply hollowed-out subcylindrical cavities (Fig. 6.4H–K), but information on how these are formed is vague. Pope (1953) indicated that the diogenid Cancellus typus lived in self-made burrows. In contrast, Mayo (1973) suggested that Cancellus species did not initially excavate their homes but instead used the rasps of their fourth and fifth pereopods and uropods to wear away the inner surfaces to enlarge the cavities as needed. To date, there is no direct evidence that any of these petricolous taxa independently hollow out their burrows. As previously indicated, occupants of these domiciles were thought to be incapable of movement because of their heavy, clumsy dwellings. However, specimens of Cancellus in the laboratory were observed to carry their stone carcinoecia with them as they explored their enclosure (Pope 1953), moved in response to food (Mayo 1973), or when engaging in shell fighting (Hazlett 1969). Additionally, several specimens of a Philippine Cancellus species reportedly were captured by tangle nets (McLaughlin 2008), as were specimens of the xylicolous pylochelid Xylocheles macrops (McLaughlin and Lemaitre 2009), which strongly suggests mobility on the part of these hermit crabs despite their cumbersome abodes. Xylopagurus species, which occupy hollows in bamboo, also are capable of movement without abandoning their carcinoecia, having been observed moving around a ship’s deck following capture (R. Lemaitre, personal communication). Tanaidacea The Tanaidacea is an order of generally tiny peracaridan crustaceans that, despite their small size, are important and abundant members of many benthic communities. Most are burrowers or builders of tubes affixed to the substratum. But, surprisingly, members of three genera, Macrolabrum, Pagurotanais, and Pagurapseudes, have gained mobility through the adoption of small gastropod shells, much like young hermit crabs. Most are shallow-water species; however, at least one is known to inhabit depths in excess of 400 m (Bamber 2007). Although the focus of most reports of these tanaids has been taxonomic, McSweeny (1982) found Pagurapseudes largoensis to be a shell generalist, with shell choice apparently based on shell characteristics. Representatives of this species showed a preference for shells with large apertures and broad body whorls. McLaughlin (1983) summarized the adaptive similarities and differences of P. largoensis and two hermit species and

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Fig. 6.4. “Alternative” housing: (A–G) Xylicolous abodes. (H–K) Petricolous accommodations. A–G, I–K, courtesy of T.-Y. Chan; H, courtesy of A.J. Provenzno, Jr.

found the most obvious shared character to be pleonal twisting. However, the loss of pleonal calcification and segmentation seen in most hermit crabs is much less in Pagurapseudes, with segmentation retained and only a gradual posteriad decrease in calcification. Bamber (2009) pointed out a unique morphological adaptation by pagurapseudids for cochlean habitation, one not seen in paguroids. This is the presence of flat-topped, rounded, “sucker-like” spines on the merus, carpus, and propodus of each of the posterior five pairs of pereopods.



Patsy A. McLaughlin

Amphipoda Amphipod crustaceans occupy a broad spectrum of environmental niches; however, one Infraorder, the Corophiida, contains many examples of domicolous species (Myers and Lowry 2003 and references therein; Fig. 6.5). These amphipods are set apart by the presence of glands in the bases of pereopods 3 and 4, which open through pores in the tips of the dactyls of these appendages. These glands produce threads that the animals use to build tubes. Just (1985) described three principal types of amphipod housing. The first, the self-constructed tubes for permanent residence, are attached directly to the substratum and do not afford mobility. However, among the siphonoecetins, many members occupy mobile homes. These may be strong tubes that can be carried around and attached temporarily in good locations for feeding. When the food supply is depleted, the amphipods detach their tubes and move to other locations. Other siphonoecetins affix their tubes to empty gastropod and scaphopod shells, while still others occupy empty shells or the tubes of polychaete worms without additional tubes of their own construction. Interestingly, shells of the pteropod Cuvierinia columnella are utilized by species of the paguroid genus Pteropagurus and the amphipod genus Pterunciola, both having been named for this distinctive carcinoecium. Among the hyperiidean amphipods, Hyperiella dilatata grabs the pteropod Clione limacina with its pereopods and carries it dorsally, most likely as a chemical defense shield (McClintock and Janssen 1990). Although hermit crabs and amphipods are capable of moving large and awkward abodes, hermit crabs walk using pereopods 2 and 3, whereas the locomotory appendages of amphipods are their very stout antennae. Despite the variety of carcinoecia adopted by hermit crabs, certain amphipods have taken this evolutionary innovation a step further. One species, Pseudamphithoides incurvaria, constructs its domicile from two equal oval-shaped thin pieces of brown algae. The pieces are doubled over and glued together, leaving slit-like openings at either end. As the amphipod moves about among

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Fig. 6.5. (A) Drawing made from preserved material showing two gastropod shells inhabited by the amphipod Photis conchicola and attached to a foliose alga. The shell-alga attachment site above the turriform shell is circled. Rule is equal to 1 mm. From Carter (1982), with permission from The Crustacean Society. (B) The amphipod Cerapus murrayae Lowry and Berents, 2005, Queenscliff Lagoon, New South Wales: (i) adult male; (ii) tube with male protruding. From Lowry and Berents (2005), with permission from Australian Museum.

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Crustaceans in Mobile Homes hydroids and algae, its “house” is carried freely in a somewhat upright position, presumably held in place by it prehensile pereopods 5–7 ( Just 1977). These mobile homes are preferentially built from brown algae of the genus Dictyota, on which P. incurvaria also feeds voraciously (Lewis and Kensley 1982). When offered a choice of different algal species, they prefer those species of Dictyota that offer chemical defense against fish predators (Hay et al. 1990). Recently born juveniles remain in the domicile of the female for an unspecified period of time (Lewis and Kensley 1982), thus enjoying the protection (and food) in their mother’s mobile home. Species of Cerapus builds tight-fitting tubes, and although individuals occasionally attach their mobile tubes to algae and other substrata, they frequently move around in them. In particular, the males seem to roam in search of receptive females among the dense assemblages of conspecifics (Barnard et al. 1991). Males of Siphonoecetes dellavallei even glue the tubes of females to their larger tubes and thus carry a small harem around with them (Richter 1978). Other species utilize hollow stem nodes from sea grass or transparent polychaete tubes, or they construct “houses” using bits of sea grass and algae. Using downward strokes of their plumose antennae, these amphipods can swim rapidly while carrying their homes (Barnard et al. 1991).

FUTURE DIRECTIONS Much experimental research remains to be done regarding shell choice of hermit crabs. Many factors have been identified as being important for a hermit crab to decide if a shell is a good fit, and preferences for shell types are usually apparent. However, the ranges of shells (whether they are from gastropods, bivalves, pteropods) that hermit crabs are willing to accept still need to be clarified for many species. This is especially important for understanding how hermit crabs adapt when they find themselves outside of their usual range or are confronted with a scarcity of their preferred shell. Also, it remains to be confirmed whether those species with wood and stone dwellings would prefer the shells outlined above if provided to them. There are several aspects of the relationship between hermit crabs and their symbionts that remain a mystery. Many of these relationships have been disputed, especially regarding whether symbionts erode hermit crab shells, serve to enlarge them, or provide optimal living conditions for the crabs, and whether hermit crabs will opt to use shells with these organisms for long-term occupancy. Few consistent patterns have emerged concerning the benefits of the symbionts to hermit crabs and vice versa. For some species, it has been suggested that hermit crabs inhabit shells with symbionts as a last resort and would normally prefer a “clean” shell (Sandford 2003). The latter question and others concerning the relationship between hermit crabs and their symbionts leave noticeable gaps in our knowledge that can be closed with experimental research. Last, research on mobile homes has been highly focused on hermit crabs. Members of Tanaidacea and Amphipoda should be examined to understand their specific adaptations and be compared to the more extensive knowledge about hermit crabs. Perhaps by studying these groups, which differ very much from hermit crabs, we may come to a fuller understanding of the use of mobile homes in crustaceans.

CONCLUSIONS Hermit crabs have developed a particular lifestyle in which they literally sport their homes on their “backs,” at times carrying shells that are many times their own weight. To be able to fit into these shells, hermit crabs have developed an asymmetric pleon that is believed to have evolved from



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an ancestor similar to a pylochelid, as the paguroids adapted to different kinds of shelters (van Bakel et al. 2008). The most common type of shell for hermit crabs is obtained from dead gastropods. Finding a good shell is paramount for hermit crabs, and a decision regarding a shell is made depending on size, weight, overall condition, aperture shape, and, sometimes, color, shell specificity, and presence or absence of epibionts (Mercando and Lytle 1980, Brooks and Mariscal 1985, Lizka and Underwood 1990, Tricarico and Gherardi 2006). A good shell is highly prized, and thus one can occasionally observe patterned agonistic behavior in which one hermit crab dislodges another crab and inhabits the new shell. Although gastropod shells are the most common choice, some hermit crabs inhabit scaphophod (tusk) shells. Several families of hermit crabs have developed straighter pleons, among other adaptations, to better fit the form of these shells. Hermit crabs that occupy halves of bivalve shells are even less numerous because they require more extreme morphological adaptations. Similarly, few hermit crabs utilize pteropod mollusk shells. A key problem for hermit crabs is that any increase in body size also requires a larger domicile. As a result of this problem, some adaptations have arisen, such as symbiotic housing. In symbiotic housing, hermit crabs receive the aid of epifaunal symbionts. These organisms, which generally come from the invertebrate phyla Porifera, Cnidaria, and Bryozoa, may live in, on, or around the shell, and sometimes even replace the shell itself. In some cases, hermit crabs literally “wear” these symbionts, which may act as a sack-like protective layer, entirely doing away with the need for a shell. Another alternative to shells or symbiotic housing are xylicolous (wood) and petricolous (stone) dwellings. The crabs often wear away and smooth out the wood and stone to fit their bodies. Although they may seem clumsy because of their weight and shape, hermit crabs that inhabit these structures are surprisingly mobile. Last, there are other crustaceans in addition to hermit crabs that use mobile homes. Some members of Tanaidacea use small gastropod shells, and some amphipods are also domicolous. Ampithoid and corophiid amphipods have glands that produce threads, allowing them to create their own homes and attach to shells or other substrata.

ACKNOWLEDGMENTS The author acknowledges with gratitude the permissions granted to utilize their photographs in this presentation by numerous colleagues listed in the figure legends. Special thanks belong to George P. Holm (Richmond, BC, Canada) for his professional presentation of these figures.

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Crustaceans in Mobile Homes McLaughlin, P.A., R. Lemaitre, and U. Sorhannus. 2007. Hermit crab phylogeny: its reappraisal and its “fallout.” Journal of Crustacean Biology 27:97–115. McSweeny, E.S. 1982. A new Pagurapseudes (Crustacea: Tanaidacea) from southern Florida. Bulletin of Marine Science 32:455–466. Mercando, N.A., and S.F. Lytle. 1980. Specificity in the association between Hydractinia echinata and sympatric species of hermit crabs. Biological Bulletin 159:337–348. Myers, A.A., and J.K. Lowry. 2003. A phylogeny and a new classification of the Corophiidea Leach, 1814 (Amphipoda). Journal of Crustacean Biology 23:443–485. Partridge, B.L. 1980. Background camouflage: an additional parameter in hermit crab shell selection and subsequent behavior. Bulletin of Marine Science 30:914–916. Pope, E.C. 1953. Stones that walk. Australian Museum Magazine 11:44–46. Provenzano, A.J., Jr. 1971. Rediscovery of Munidopagurus macrocheles (A. Milne-Edwards, 1880) (Crustacea, Decapoda, Paguridae), with a description of the first zoeal stage. Bulletin of Marine Science 21:256–266. Richter, G. 1978. Einige Beobachtungen zur Lebensweise des Flohkrebses Siphonoecetes della-vallei. Natur und Museum 108:259–266. Richter, S., and G. Scholtz. 1994. Morphological evidence for a hermit crab ancestry of lithodids (Crustacea, Decapoda, Anomala, Paguroidea). Zoologischer Anzeiger 223:187–219. Rittschof, D. 1980. Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. Journal of Chemical Ecology 6:103–118. Rodrigues, L.J., D.W. Dunham, and K.A. Coates. 2000. Shelter preferences in the endemic Bermudian hermit crab, Calcinus verrilli (Rathbun, 1901) (Decapoda, Anomura). Crustaceana 73:737–750. Ross, D.M. 1974. Evolutionary aspects of associations between crabs and sea anemones. Pages 111–125 in W.B. Vernberg, editor. Symbiosis in the sea. University of South Carolina Press, Columbia. Sandford, F. 2003. Population dynamics and epibiont associations of hermit crabs (Crustacea: Decapoda: Paguroidea) on Dog Island, Florida. Memoirs of Museum Victoria, 60:45–52. Sandford, F., and C. Brown. 1997. Gastropod shell substrates of the Florida hermit-crab sponge, Spongosorites suberitoides, from the Gulf of Mexico. Bulletin of Marine Science 61:215–223. Schijfsma, K. 1935. Observations on Hydractinia echinata (Flem.) and Eupagurus bernhardus (L.). Archives Neerlandaises de Zoologie 1:161–214. Scully, E.P. 1983. The behavioral ecology of competition and resource utilization among hermit crabs. Pages 23–55 in S. Rebach and D.W. Dunham, editors. Studies in adaptation: the behavior of higher Crustacea. J. Wiley and Sons, New York. Smith, A.G. 1969. Staghorns and longhorns. Pacific Discovery 19:30–31. Taylor, P.D. 1991. Observations on symbiotic associations of bryozoans and hermit crabs from the Otago shelf of New Zealand. Vol. 1. Pages 487–495 in F.P. Bigey, editor. Bryozoaires actuels et fossiles: Bryozoa living and fossil. Bullétin de Société Naturelle Quest Française, Mémoires, HS. Taylor, P.D., P.J. Schembri, and P.L. Cook. 1989. Symbiotic associations between hermit crabs and bryozoans from the Otago region, southeastern New Zealand. Journal of Natural History 23:1059–1085. Tricarico, E., and F. Gherardi. 2006. Shell acquisition by hermit crabs: which tactic is more efficient? Behavioural Ecology and Sociobiology 60:492–500. Vafeiadou, A.M., C. Antoniadou, and C. Chintiroglou. 2012. Symbiosis of sea anemones and hermit crabs: different resource utilization patterns in the Aegean Sea. Helgoland Marine Research 66:385–392. van Bakel, B.W.M., R.H.B. Fraaije, J.W.M. Jagt, and P. Artal. 2008. An unexpected diversity of Late Jurassic hermit crabs (Crustacea, Decapoda, Anomura) in Central Europe. Neues Jahrbuch für Geolgie und Paläontologie 250:137–156. van Soest, R.W.M. 1993. Distribution of sponges on the Mauritanian continental shelf. Hydrobiologia 258:95–106. Vermeij, G.J. 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3:245–258. Wells, H.W. 1969. Hydroid and sponge commensals of Cantharus cancellarius with a “false shell.” Nautilus 82:93–102. Williams, J.D., and J.J. McDermott. 2004. Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology 305:11–128.

7 CRUSTACEANS AS SYMBIONTS: AN OVERVIEW OF THEIR DIVERSITY, HOST USE, AND LIFESTYLES

J. Antonio Baeza

Abstract The adoption of a symbiotic lifestyle is a major adaptation in the marine realm. Protection against environmental stress, escape from natural enemies, and nourishment are the major benefits obtained by symbiotic crustaceans from hosts. Hosts also represent a mating and nursery ground for symbiotic crustaceans. Costs and/or benefits experienced by hosts are diverse but may be subtle and challenging to measure. Costs suffered by hosts include physical injury, reduced feeding/growth rates, decreased fecundity and lifespan, and feminization, including castration, of male hosts. Some rhizocephalans are capable of altering host behaviors. The life cycles of symbiotic crustaceans vary widely. At one extreme, juveniles recruit directly into hosts from parental brooding chambers in crustaceans with direct/abbreviated development. Many symbiotic crustaceans with indirect development spend their larval life in the pelagic environment and establish themselves in/on their hosts during the first post-larval stage. At another extreme, the most complex life cycles occur in parasitic copepods and rhizocephalan cirripedes. Such life cycles involve one or two hosts and subtle or considerable changes in body morphology relative to that of their closest free-living relatives. The species richness of various symbiotic clades is higher than that of their closest free-living relatives. Whether the symbiotic lifestyle favors adaptive radiations in crustaceans is an outstanding and open question.

INTRODUCTION The adoption of a symbiotic lifestyle (symbiosis here is defined sensu De Bary [1879] as dissimilar organisms living together) is one of the most important environmental adaptations in marine organisms (Ross 1983, Vermeij 1983). Symbiotic associations in the marine realm usually comprise

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Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles small organisms (hereafter symbiotic guests) and large partners that serve as hosts. Symbiotic relationships can be characterized in terms of the costs and benefits experienced by the partners (i.e., parasitism, commensalism, mutualism), the degree of interdependency among the associates (i.e., facultative or obligate symbiosis), the number of species used by one or both entities involved in the symbiotic interaction (i.e., generalists vs. specialists), and the location or physical area in or on hosts exploited by symbiotic guests (endosymbionts, ectosymbionts, mesosymbionts, cohabitants; Bush et al. 1997, Thiel and Baeza 2001). In marine crustaceans, some degree of dependence between pairs or among small assemblages of species has evolved multiple times independently in tropical, subtropical, and temperate habitats

A

B

Fig. 7.1. Two examples of symbiotic crustaceans. (A) The caridean shrimp Lysmata pederseni, a socially monogamous and protandric simultaneously hermaphroditic species inhabiting the vase sponge Callyspongia vaginalis. Photo courtesy of Raphael Ritson-Williams. (B) The isopod Cymothoa exigua. This species causes the degeneration of most of the tongue of its host fish, the snapper Lutjanus guttatus. From Brusca and Gilligan (1993), with permission from the American Society of Ichthyologists and Herpetologists.



J. Antonio Baeza

(Bruce 1976, Castro 1971, 1976, Ross 1983, Thiel and Baeza 2001). Species of caridean shrimps, pentastomids, tantulocarids, crabs, amphipods, isopods, mysids, cirripedes, and copepods (among others) from dissimilar monophyletic clades have been reported to engage in symbiotic associations with other macroinvertebrates, including sponges, corals, sea anemones, oysters, sea urchins, and ascidians, and with reptiles and mammals (Bruce 1976, Castro 1976, Ross 1983, Tappe and Büttner 2009; Fig. 7.1). Crustaceans are among the most diverse marine invertebrates (Brusca and Brusca 2003), and the studies conducted during the past decades in symbiotic representatives of this species-rich group have revealed most impressive morphologies (Schmitt et al. 1973, Fransen 2002), colorations (Limbaugh et  al. 1961), nourishment tactics (Ďuriš et  al. 2011), reproductive strategies (Shuster and Wade 1991), social systems (Duffy et al. 2000), parent–offspring interactions (Thiel 2003), and modes of interspecific communication (Vannini 1985, Becker et al. 2005). This chapter reviews the diversity of symbiotic crustaceans. An overview of the cost and benefits experienced both by crustaceans and their partners and the life cycle of symbiotic crustaceans is provided.

SYMBIOTIC CRUSTACEANS AND THEIR HOST PARTNERS The systematic arrangement laid out by Martin and Davis (2001) is used as a main framework to explore the incidence of symbiosis in the Crustacea. This review revealed no instances of symbiosis in members from the classes Remipedia (remipedes) and Cephalocarida (horseshoe shrimps). Their anchihaline lifestyle (Remipedia) and/or meiofaunal habitat (Cephalocarida) might prevent the evolution of symbiosis in these clades (Neiber et al. 2011). In the morphologically and ecologically diverse class Branchiopoda (cladocerans or “water fleas” and fairy, brine, tadpole, and clam shrimps), members from all orders but one are free-living. Only a few species in the order Diplostraca, suborder Cladocera, family Chydoridae, have been considered parasites of freshwater cnidarians (Hydra spp.). For instance, Anchistropus minor and A.  emarginatus have strong hooks on the first pair of limbs that are used for shredding ectodermal cells from regions of polyps other than their cnidocyte-rich tentacles (Hyman 1926, Fryer 1968). However, some authors considered these species to be predators because they are lethal to their “hosts” and can quickly destroy an entire population of Hydra in short periods of time (Van Damme and Dumont 2007). In the diverse class Malacostraca, this review revealed no instances of symbiosis in the subclass Phyllocarida (leptostracans). However, in the subclass Eumalacostraca, the symbiotic lifestyle is pervasive in the superorder Eucarida, order Decapoda (e.g., shrimps, brachyuran crabs, squat lobsters, hermit crabs) and in the superorder Peracarida (e.g., amphipods, isopods, mysids). In the order Decapoda, groups that have adopted a symbiotic lifestyle include stenopodid shrimps (Infraorder Stenopodidea) in the family Spongicolidae (e.g., Globospongicola) that live entrapped in the atrium of deep-water hexactinellid sponges (Saito and Takeda 2003, Saito and Komai 2008; Fig. 7.2A). In the infraorder Caridea, pontonid shrimps (superfamily Palaemonoidea, subfamily Pontoniidae) from diverse genera engage in obligatory ecto- or endosymbiotic associations with a wide variety of hosts, including, sponges, hydrozoans, sea anemones, jellyfish, black corals, sea pens, echinoderms, mollusks, and ascidians (Bruce 1982, De Grave 1999, Fransen 2002, 2006). In the Infraorder Brachyura (true crabs), the symbiotic lifestyle is also widespread. In the superfamily Trapezioidea, most genera (e.g., Trapezia, Tetralia) are obligate ectosymbionts of hydrozoan stylasterid corals, gorgonian and alcyonacean corals, scleractinian corals, and antipatharian corals (Castro 1976, Castro et al. 2004). Also, crabs in the superfamily Cryptochiroidea are obligate

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Fig. 7.2. Diversity of symbiotic crustaceans. (A) Globospongicola spinulatus, a stenopodid shrimp (Stenopodidea) in the family Spongicolidae that lives entrapped in the atrium of deep-water hexactinellid sponges. From Komai and Saito (2006), with permission from Publications Scientifiques du Muséum national d’Histoire naturelle, Paris. (B) Tunicotheres moserii, a pea crab (Brachyura, Pinnotheroidea) with abbreviated development living in the atrial chamber of various ascidians in the Caribbean. From Campos (1996), with permission from The Crustacean Society. (C) Dorsal (left) and ventral (right) view of the whale-lice Cyamus ovalis (Cyamidae) that attach to the skin of the right-whale Balaena gracialis. From Iwasa (1934), with permission from Hokkaido Imperial University. (D) Hyperia galba, an amphipod (Peracarida) developing obligate symbiosis with gelatinous zooplankton. From Sars (1899). (E) Dorsal view of the female (left) and micrography of the male (in ventral view, right) of Orthione griffenis (Bopyridae), a parasitic isopod of thalassinid mud shrimps found in the north Pacific. From Williams and An (2009), with permission from Oxford University Press. (F) Ceratothoa gaudichaudii (Cymothoidae), an associate of various pelagic fish in the southeastern Pacific. From Brusca (1981), with permission from John Wiley and Sons. (G) Dorsal view of the adult male (left) and adult female (right) of Gnathia maxillaris. From Sars (1899). (H) Praniza larva of Gnathia maxillaris, an ectoparasite of the marine fish Blennius pholis. From Sars (1899). Scale bars or magnifications: A and B = 2 mm; C = 4.2×; D and E = 1 mm; D, G, and F, not available.



J. Antonio Baeza

symbionts of scleractinian corals. These crabs live in self-constructed “galls” or open “pits” that they excavate in corals. The interiors of these structures are lined with living coral tissue (Scotto and Gore 1981). Last, the superfamily Pinnotheroidea (pea crabs) is recognized for its symbiotic lifestyle. Most species from the 55 currently recognized genera (e.g., Zaops, Pinnotheres, Tunicotheres) have developed some degree of dependence with a wide variety of hosts, primarily bivalves, gastropods, equinoderms, polychaetes, equiurid worms, and ascidians (Schmitt et al. 1973; Fig. 7.2B). Some species even use burrows constructed by other crustaceans as a refuge (e.g., Austinixa patagonensis in burrows of the ghost shrimp Sergio mirim; Harrison 2004). In the species-rich superorder Peracarida, many members from the orders Isopoda and Amphipoda have adopted a symbiotic lifestyle. Species from the other orders (e.g., Cumacea, Tanaidacea, and others) are almost invariably free living. One notable exception is Heteromysis harpax (order Mysida), which forms family groups in the interior of gastropod shells occupied by hermit crabs (Vannini et al. 1994). In the order Amphipoda, members from the suborder Caprellidea, family Cyamidae (whale-lice) cling to the external surface of whales and dolphins (Gruner 1975) (Fig. 7.2C), whereas many species in the suborder Hyperiidea are obligate symbionts of cnidarians, salps, and other gelatinous zooplankton (e.g., Hyperia galba; Sars 1899, Laval 1980, Vinogradov et al. 1996; Fig. 7.2D). Other amphipods symbiotic within sponges and tunicates pertain to the families Dexaminidae and Leucothoidae. Another 22 species from seven different families are also considered ecto- or endosymbiotic or micropredators of sea anemones (Vader 1983). In the order Isopoda, the suborder Epicaridea is exclusively symbiotic (parasitic, see below) with other crustaceans. The diverse family Bopyridae inhabit the visceral cavity, branchial chamber, or abdominal surfaces of a diverse number of benthic decapods and pelagic mysidaceans and euphausiaceans (Kensley and Schotte 1989; Fig. 7.2E). In turn, the suborder Flabellifera is mostly free-living but a few groups within this clade have adopted a symbiotic lifestyle. Among them, the family Cymothoidae is recognized for its obligatory relationship with fishes (Bunkley-Williams and Williams 1998; Fig. 7.2F). Also, a few species in the family Corallanidae have been collected from the gills of bony fishes, nurse sharks, and rays (e.g., Alcirona insularis, Excorallana tricornis tricornis) or from the surface of corals (e.g., E. tricornis tricornis). Also in the Flabellifera, members of the family Aegidae might be considered symbiotic because they temporarily attach to marine fishes (or rarely humans) to feed on their blood (e.g., Rocinela signata). However, specimens from this family are most frequently captured by relatively deep bottom trawls (Brusca 1983). Last, various members from the family Sphaeromatidae are found under chitons (e.g., Dynamenella perforata) or use sponges for breeding (e.g., Paracerceis sculpta; Shuster and Wade 1991). In the suborder Gnathiidae, adult specimens do not feed and are found in cavities available in the mud, dead barnacles, corals, or sponges (Kensley and Schotte 1989). However, the early ontogenetic stages temporarily attach to fish (Lester 2005; Fig. 7.2G,H). Symbiosis is absent or is much less common in the suborders Anthuridea, Asellota, Oniscoidea, Microcerberidea, and Valvifera. However, a few species from these clades have been collected from the surface of corals or sponges (Asellota: Joeropsis coralicola from the corals Oculina arbuscula, Madracis sp., and the sponge Agelas sp.) or from crinoids (Valvifera: Astacilla regina; Kensley and Schotte 1989). In the species-rich and morphologically diverse but comparatively poorly studied class Maxillopoda (e.g., barnacles, copepods, tongue-worms, fish-lice), the symbiotic mode of life is pervasive. In the subclass Thecostraca (barnacles and allies), symbiosis is obligatory in three major taxa, the infraclasses Ascothoracida and Facetotecta and the subclass Rhizocephala in the infraclass  Cirripedia (Høeg et  al. 2005). Members from the Ascothoracida are ecto- and endosymbiotic with cnidarians and echinoderms (Fig. 7.3A–C). Laboratory observations suggest that the enigmatic Facetotecta are endosymbiotic too, having an invasive stage similar to that of rhizocephalan cirripedes. However, the natural hosts of this group are not known (Grigyer 1987,

167

Fig. 7.3. Diversity of symbiotic crustaceans. (A)  External view of the brittle star Ophiocten sericeum infected with Ascothorax ophioctenis (Ascothoracida). The arrow points at the endosymbiont. From Wagin (1946), with permission from John Wiley and Sons. (B)  Male (m)  and female (f, dorsal view) of Ascothorax ophioctenis after extraction from the host. From Wagin (1946), with permission from John Wiley and Sons. (C)  Male of Ascothorax ophioctenis after separation from the female. From Wagin (1946), with permission from John Wiley and Sons. (D) Sacculina carcini (Rhizocephala), an endoparasite of various brachyuran crab. Notice the extreme body modification. From Haeckel (1899). (E) Coronula reginae (Thoracica), a sessile barnacle that lives attached to the right whale Eubalaena glacialis. From Haeckel (1899). (F) The copepod Cryptopontius thorelli (Siphonostomatoida), ectoparasitic on the sponge Petrosia ficiformis. From Haeckel (1899). (G) Inner view of the oral pole of the sea urchin Hygrosoma petersii showing calcified galls containing the copepod Pionodesmotes



J. Antonio Baeza

Glenner et al. 2008). In turn, members from the Rhizocephala are highly modified and commonly use decapod crustaceans as hosts (Fig. 7.3D) and, less frequently, have been retrieved from species of Cumacea (Peracarida), Stomatopoda, and few free-living barnacles in the subclass Thoracica (Cirripedia). Also in the Cirripedia, members from the superorder Acrothoracica excavate burrows in calcareous material, including corals, crinoids, or gastropod shells used by hermit crabs (Williams and McDermott 2004). In turn, sessile cirripedes in the superorder Thoracica, superfamily Coronuloidea, attach to the body of whales (e.g., Coronula reginae, Scarff 1986) and turtles (e.g., Chelonibia testudinaria, Frick and Ross 2001; Fig. 7.3E). In the class  Maxillopoda, subclass  Copepoda, symbiosis is obligatory in three orders, the Monstrilloida, Poecilostomatoida, and Siphonostomatoida. In the Monstrilloida, the naupliar, preadult, and adult phases are planktonic but during their postnaupliar and juvenile phases, they are endosymbiotic with gastropods, polychaetes, or, rarely, with equinoderms (Suárez-Morales 2011). Members of the Poecilostomatoida are usually ectosymbiotic and find refuge on the buccal cavity of mollusks and equinoderms or gills of bony fishes. However, three genera (Clavisodalis, Echinirus, and Echinosocius) in this clade have adopted an endosymbiotic lifestyle living in the esophagus of sea urchins (Dojiri and Cressey 1987). Members of the Siphonostomatoida parasitize invertebrates and fishes (Barel and Kramers 1977; Fig. 7.3F–H). One order, Calanoida, is mostly free-living. However, several species from this order have adopted a symbiotic lifestyle. The other two orders, Cyclopoida and Harpacticoida, contain relatively large and moderate numbers of symbiotic species, respectively. Last, the most aberrant symbiotic species pertain to the class  Maxillopoda, subclasses Tantulocarida and Pentastomida. Tantulocarids are minute parasites of deep-sea benthic crustaceans that exhibit a highly modified adult form (Boxshall and Lincoln 1983; Fig. 7.3I,J). Pentastomids (tongue-worms) are larger parasites than tantulocarids, have a worm-like body shape, and dwell on the respiratory tracts of reptiles, birds, and mammals, including humans (Lavrov et al. 2004, Tappe and Büttner 2009; Fig. 7.3K). Much less aberrant, the Branchiura (fish lice) live on the external surface of marine and freshwater fish and amphibians (Fig. 7.3L). Examples are Argulus coregoni infecting the rainbow trout Oncorhynchus mykiss (Bandilla et al. 2005) and A. ambystoma infecting the salamander Ambystoma dumerilii (Poly 2003).

BENEFITS TO SYMBIOTIC CRUSTACEANS DERIVED FROM HOSTS Protection against environmental stress and/or escape from natural enemies (e.g., predators and competitors) appear to be the major benefits that symbiotic crustaceans obtain from their respective hosts (Table 7.1). This is certainly true for endosymbiotic species developing obligatory symbioses. Highly modified crustaceans inhabiting host cavities (e.g., pea crabs and rhizocephalan cirripedes; Figs. 7.2 and 7.3) would probably die within minutes or hours if deprived from their host Fig. 7.3.  (Continued) phormosomae (Poecilostomatoida). From Koehler (1898) in Jangoux (1987). (H) Section through gall harboring a female of Pionodesmotes phormosomae and also showing the outer pore of the gall (P). From Bonnier (1898) in Jangoux (1987). (I) Female of Microdajus langi (Tantulocarida) attached to the gnathid Leptognathia breviremis (shown in ventral view). From Boxshall and Lincoln (1987), with permission from Royal Society. ( J) Juvenile tanaid peracarid with two early stage female Microdajus langi. From Boxshall and Lincoln (1987), with permission from Royal Society. (K) Various exceptionally preserved specimens of fossil Pentastomida (from CORE; available at http://www.core-orsten-research.de). (L) Dorsal (left) and ventral (right) view of Argulus quadristriatus (Branchiura), symbiotic with the marine fish Psammoperca waigiensis. From Devaraj and Hamsa (1977). Scale bars. H = 1 mm; J = 200 micrometers; K = 500 micrometers, M = 2 mm.

169

Table 7.1.  Host use patterns in symbiotic crustaceans Taxa C. Branchiopoda O. Diplostraca C. Malacostraca S.C. Eumalacostraca S.O. Peracarida O. Mysida O. Amphipoda O. Isopoda S.C. Eucarida O. Decapoda C. Maxillopoda S.C. Thecostraca I. Facetotecta I. Ascothoracida

Symbiosis

Hosts

Location

Food

Type

Specificity Mobility

Sociality

Rare

Cnidaria

Ec

HostT

P

?

High

?

Rare Frequent Frequent

Hermit crabs Many Many

Coh Ec, En, Coh Ec, En, Coh

HostT HostT, I HostT, I

M? P, C P, C

? L to H L to H

L to M L to M L to M

Fam Unstr, Fam, Str Unstr, Fam, Str

Frequent

Many

Ec, En, Coh

HostT to I

P, C, M

L to H

None to H

Unstr, Fam, Str

Obligatory? Obligatory

Unknown Cnidaria, Echinodermata

Ec, En

HostT to I

P

L to H?

None

Str

I. Cirripedia S.O. Acrothoracica

Rare

Ec, Coh

D, I

C

L to H

None

Str

S.O. Rhizocephala

Obligatory

En

HostT

P

L to H

None

Str

S.O. Thoracica S.C. Tantulocarida

Rare Obligatory

Ec Ec

D, I D, I

P, C P, C

L to H L

None None

Unstr Unstr

S.C. Branchiura

Obligatory

Corals, hermit crab shells Decapoda, Peracarida Whales, Turtles Peracarida, Ostracoda Fish

Ec

D, I

P, C

H

M to H

Unstr

S.C. Pentastomida

Obligatory

Reptiles, Birds, Mammals

En

D, I

P, C

?

None

Unstr

S.C. Copepoda O. Calanoida O. Cyclopoida O. Harpacticoida O. Monstrilloida

Frequent Frequent Frequent Obligatory

Ec Ec Ec En

? ? ? HostT

P, C P, C P, C P

L to H L to H L to H L to H?

L to M L to M L to M None

Unstr Unstr Unstr Str

O. Poecilostomatoida

Obligatory

Ec, En

HostT

P

L toH?

None

Str

O. Siphonostomatoida

Obligatory

Many Many Many Gastropoda, Polychaeta Gastropoda, Equinodermata, Fishes Many invertebrates, Fish

Ec, En

HostT

P

L toH?

None

Str

Class Ostracoda Sc. Myodocopa O. Myodocopida

Rare

Fish

Ec

HostT

P

?

?

?

The existence and extent of the symbiotic lifestyle (Symbiosis: Rare, Frequent, Obligatory) in each major clade, the hosts (Hosts) most commonly used by symbiotic crustaceans in each clade, the location or physical area in/on hosts exploited by symbiotic guests (Location: endosymbionts [En], ectosymbionts [Ec], cohabitants [Coh]), the type of nourishment and/or mode of acquisition of food by symbiotic crustaceans (Food: food not acquired directly from hosts but obtained via, for example, filter feeding [I]‌, direct from hosts [D], including the consumption of host’s tissues, waste or mucus produced by hosts [HostT]), the type of symbiotic relationships characterized in terms of the costs and benefits experienced by the partners (Type: parasitism [P], commensalism [C], mutualism [M]), the number of host species used by symbiotic crustaceans (Specificity [along the generalist—specialist continuum] from low specificity [L] to moderate [M] and high [H] specificity), the extent of mobility during the life cycle of symbiotic crustaceans (Mobility: from None to low (L) to moderate [M] to high [H] mobility), and the sociobiology of symbiotic crustaceans (Sociality: unstructured, including species living in aggregations [Unstr], family groups composed by a female and offspring or reproductive (e.g., male–female) pairs [Fam], structured, including pair-living species that do not interact with offspring, and polygamous species [Str]) are shown. These are general classifications for each clade, and several of these should be considered tentative considering the lack of studies. See text for details. Note: No symbiotic species have been reported in the class Remipedia, class Cephalocarida, orders Anostraca and Notostraca in the class Branchiopoda, subclasses Phyllocarida and Hoplocarida in the class Malacostraca, suborder Syncarida in the subclass Eumalacostraca, orders Spelaeogriphacea, Thermosbaenacea Lophogastrida, Mictacea, Tanaidacea and Cumacea in the suborder Peracarida, order Euphausiacea and Amphionidacea in the subclass Eucarida, subclass Mystacocarida in the class Maxillopoda, order Gelyelloida, Misophrioida, Mormonilloida and Platycopioida in the subclass Copepoda, and orders Halocyprida, Platycopida and Podocopida in the class Ostracoda.

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Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles individuals (killed by predators or adverse environmental conditions). Also, many ectosymbiotic crustaceans most likely gain protection against environmental stress and/or escape from natural enemies by dwelling on or near the surface of their respective hosts. Admittedly though, the actual number of experimental studies that have formally tested for the positive effect of hosts on the survival of ectosymbiotic crustacean guests is most limited (Thiel and Baeza 2001). Other than shelter, hosts provide a suite of other resources and services to symbiotic crustaceans. Among them, hosts represent an indirect or direct food source. The porcelain crab Allopetrolisthes [a.k.a. Petrolisthes] spinifrons and its sea anemone hosts represent an example of the indirect function played by hosts in the nourishment of symbiotic crustaceans. By clinging to sea anemones, porcelain crabs gain access to exposed sites in the intertidal and subtidal zones that are favorable for suspension-feeding (Valdivia and Stotz 2006; Fig. 7.4A). In turn, various other symbiotic species acquire food directly from their hosts, and, in many instances, hosts represent the only source of nourishment for symbiotic crustaceans. Examples include members from the Branchiura (e.g., Argulus spp.; Fig. 7.3L) that suck blood and/or tissue fluids by puncturing the skin of their fish and amphibian hosts. Modified mouth parts, including a styliform proboscis and mandibles with cutting edges, most likely aid in feeding (Wilson 1944). Similarly, cymothoid isopods apparently feed principally on blood, but they may consume the mucus, epithelium, and subcutaneous tissues of their host (Bunkley-Williams and Williams 1998, Leonardos and Trilles 2003; Fig. 7.4B,C). An extreme body modification in symbiotic crustaceans for acquiring nourishment from hosts is seen in the Rhizocephala (Cirripedia), which lack the rudiments of an alimentary canal and other organs and systems. These aberrant cirripedes infiltrate their hosts with a highly ramified system of rootlets with a microstructure that suggests it is used for the absorption of nutrients directly across the integument, as in a gut epithelium (Bresciani and Høeg 2001; Fig. 7.4D). Last, brachyuran crabs symbiotic with corals (superfamily Trapezioidea) use modified pereopods to “steal” mucus produced by the host colony (Knudsen 1967). Similarly, pea crabs (Pinnotheroidea) use chelipeds, pereopods, and modified mouth pieces to “steal” mucus strings that are rich in food filtered by their bivalve hosts (Calyptraeotheres sp.; Chaparro et al. 2001). In most symbiotic crustaceans, the mechanism of food acquisition is not known or is poorly understood. Hosts represent a mating ground for symbiotic crustaceans, too. For instance, numerous symbiotic crustaceans, including true crabs (McDemmott 2005), porcelain crabs (Ng and Nakasone 1993), caridean shrimps (Fransen 2002, Baeza 2010), and cymothoid isopods (Bunkley-Williams and Williams 1998) inhabit hosts as male-female pairs (in gonochoric and sequentially hermaphroditic species) or hermaphrodite-hermaphrodite pairs (in protandric simultaneous hermaphroditic shrimps; Baeza 2010; Fig. 7.1). In all these species, symbiotic individuals mate in the interior (body cavities), on the body surface, or in the vicinity of host individuals. In various species of pea crabs (Pinnotheroidea), females live solitarily in the mantle cavity of mollusks. Males appear to continuously roam among hosts in search of receptive females that are quickly mated and soon abandoned (Ocampo et al. 2012). The highly modified Rhizocephala represent a remarkable example of extreme body and sexual system modification. Females can harbor one or two minute males (or male tissue; see Høeg et al. 2005) in specialized receptacles located in the externa, a pouch-like structure that protrudes from the host’s body. Once established, these males become permanently embedded in the female tissue (Glenner et al. 2010). In these, as well as in many other obligate symbionts (e.g., pinnotherid crabs or bopyrid isopods), males are thus substantially smaller than the comparatively large females. Last, in the isopod P. sculpta, males set up territories in sponge cavities large enough to permit the cohabitation of several females at the same time (Fig. 7.4E). These females are inseminated during the breeding season (Shuster and Wade 1991). Also in this isopod, three genetically determined male morphs featuring dissimilar mating strategies coexist in the same population (Shuster and Wade 1991).

A

B

3rd Maxilliped

D C

E

F

Fig. 7.4. Benefits to symbiotic crustaceans derived from hosts. (A) The porcelain crab Allopetrolisthes (a.k.a. Petrolisthes) spinifrons perching on its sea anemone host with their usual posture (left) and when feeding with the third maxillipeds extended during filter feeding (right). From Valdivia and Stotz (2006), with permission from Journal of Crustacean Biology. (B) The parasitic isopod Mothocya epimerica (Cymothoidea) attached between the first and second branchial arches of its host, the sand smelt Atherina boyeri. From Leonardos and Trilles (2003), with permission from Inter-Research. (C) Branchial cavity of the host after the removal of the parasite. From Leonardos and Trilles (2003), with permission from Inter-Research. (D) The root system in various species of Peltogasteridae (Rhizocephala) used for the absorption of nutrients directly across the integument as in a gut epithelium. From Bresciani and Høeg (2001), with permission from John Wiley and Sons. (E) Alpha male of the isopod Paracerceis sculpta guarding a territory (a sponge cavity) harboring two females. Beta (left) and gamma (right) males can be seen closer to the territory. From Shuster (2007), with permission from Oxford University Press. (F) Female of the amphipod Peramphithoe femorata on the kelp Macrocystis pyrifera. The female has built a nest that is used by herself and her offspring. From Cerda et al. (2010), courtesy of Ivan A. Hinojosa. Scale bars: B and C = 2 mm.

174

Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles In addition to shelter, food, and a mating arena, hosts might, directly or indirectly, be used as nurseries by symbiotic crustaceans. For instance, in the enigmatic pea crab Tunicotheres moserii, dwelling in the atrial chamber of various ascidian species in the Caribbean, females exhibit abbreviated development and retain embryos, larvae, postlarvae (megalopae), and the first crab instars within their brood pouches (Hernández et  al. 2012). Interestingly, early ontogenetic stages of T. moserii do not make use of the space available within the atrial chamber of the ascidian hosts. Offspring remain protected within the abdominal “brood chamber” of females and abandon females (and hosts) during the first crab instar. In contrast, in various endosymbiotic amphipods and isopods with abbreviated or direct development, embryos that develop and hatch as advanced larvae or juveniles recruit to and remain in the parental dwelling (hosts) for relatively long periods of time (Thiel 2003). A similar situation occurs in eusocial shrimps symbiotic with sponges (Duffy et al. 2000). Figure 7.4F shows the amphipod Peramphithoe femorata on the kelp Macrocystis pyrifera. In this species, females build a nest used for protecting the offspring. The lifestyle of herbivore crustaceans living on algal hosts is treated in a separate chapter by Veijo Jormalainen (see Chapter 18 in this volume). It is generally assumed that growing offspring remain in the parental dwelling because the chances of finding unoccupied hosts are very limited, and the risk of falling prey to predators is high (Duffy 2007, Thiel 2007, Hernández et al. 2012). Whether larvae and/or juveniles are actively or passively fed, defended, and groomed by parental individuals in these species remains to be addressed.

COSTS AND BENEFITS DERIVED BY HOSTS FROM SYMBIOTIC CRUSTACEANS Costs and/or benefits to hosts resulting from their interaction with symbiotic crustaceans might be obvious in cases where crustaceans are obligate symbionts, but are much more subtle and challenging to measure in facultative symbionts. Costs are usually severe for organisms that host highly modified endosymbiotic crustaceans. Effects of the Rhizocephala on their hosts include castration, morphological and behavioral feminization of male hosts, diminished growth rate, and full arrest of the molt cycle (Høeg et al. 2005). Some rhizocephalans also appear capable of altering the behavior of their hosts, which can be beneficial for these crustacean symbionts but detrimental to the hosts. For instance, males of the swimming crab Charybdis longicollis infected with Heterosaccus dollfusi are less aggressive than uninfected males during agonistic encounters. Diminished aggressiveness in males might avoid injury and enhance the life expectancy of the host and parasite (Innocenti et al. 2003) while likely reducing the reproductive success of the hosts. Also, the presence and feeding activities of pea crabs (Pinnotheroidea) cause gill injuries and reduce feeding rates and body condition, among other issues, and ultimately impact the growth rate and reproduction of host individuals (Stauber 1945, Bierbaum and Shumway 1988, Narvarte and Saiz 2004, Sun et  al. 2005; Fig. 7.5A). In some hosts, the mere presence of crab symbionts appears to be sufficient for halting female reproduction, as demonstrated by implantation of crab mimics (Chaparro et al. 2001; Fig. 7.5B–E). The effect of ectosymbiotic crustaceans on hosts can also be deleterious and severe. For instance, symbiotic copepods in the family Caligidae are known to affect the growth, fecundity, and survival of their fish hosts ( Johnson et al. 2004 and references therein). These copepods may also serve as vectors of viral and bacterial diseases to cultured fishes (Nylund et al. 1994). Feeding and attachment of isopods from the family Cymothoidae also cause diverse effects on their fish hosts, including behavioral changes, skin and/or gill damage (Figs. 7.1 and 7.4B,C), and increased basal metabolism, which ultimately affect condition (body weight and size), growth rate, and life span (Adlard and Lester 1994, Östlund-Nilsson et al. 2005). Some species are reported to cause anemia

A

B

100

C

Brooding Snails (%)

50

100

D

50

100

F

E

50

Coral Growth (d−1, ×10−3)

0

0

3 Weeks

5

G 3

Trapezia Present

Tra pez ia 1

Ab sen t

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Fig. 7.5. (A) The effects of the endosymbiotic pea crab Pinnotheres novaezelandiae on the green-lipped mussel Perna canaliculus include lower total wet weight and meat yield, as well as changes in shell dimensions. From Trottier et al. (2012), with permission from Elsevier. (B) The endosymbiotic pea crab Tumidotheres maculatus in the mantle cavity of the bivalve Ostrea puelchana. The white arrow points at the pea crab, from Doldan et al. (2012), with permission from Latin American Journal of Aquatic Research. (C–E) The effect of the pea crab Calyptraeotheres sp. on the reproduction of the slipper limpet Crepidula fecunda. From Chaparro et al. (2001), with permission from Elsevier. (C) Shows the percentage of brooding females after removal of egg capsules and introduction of a pea crab. (D) Shows the same response by C. fecunda after removal of egg capsules and introduction of a pseudo-pea crab (a pinnotherid-sized piece of Parafilm). (E) Shows the percentage of brooding females after elimination of a pinnotherid (* = no incubation occurred; for experiment details, see Chaparro et al. (2001)). (F)  Trapezia crab defending its coral host, Pocillopora damicornis, from a crown-of-thorns starfish. From Pratchett et al. (2000), with permission from Springer. (G) Effect of the vermetid snail Dendropoma maximum and the symbiotic crab Trapezia serenei on the growth rate of Pocillopora cf. verrucosa (means ± 1 SE). From Stier et al. (2010), with permission from Springer; see Stier et al. (2010) for experiment details. Scale bars: B = 10 mm.

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Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles in their hosts (Horton and Okamura 2003). However, the impact of other cymothoid isopods on fish hosts appears to be null or minimal (Colorni et al. 1997). Symbiotic associations also result in benefits to hosts, although these are less commonly reported. The caridean shrimp Alpheus lottini and crabs from the genus Trapezia defend their coral hosts (Pocillopora elegans) from predatory sea stars Acanthaster planci in the tropical east Pacific (Glynn 1980). Similarly, the shrimp Alpheus cf. armatus defends its sea anemone host Bartholomea annulata from the predatory worm Hermodice canuculata (Polychaeta) in the Caribbean (Smith 1977). In the Indo-Pacific, crabs from the genus Trapezia and Tetralia also defend their coral colonies from predatory sea stars (Pratchett et al. 2000; Fig. 7.4F) and remove the mucus produced by the vermetid gastropod Dendropoma maximum that also dwells among the host corallites. The mucus of this snail is deleterious to corals (Stier et al. 2010), and mucus removal by crabs positively affects the growth rates of their hosts (Fig. 7.5G). Trapezia and Tetralia crabs can and do discard sediments deposited on the coral surface of their host individuals and are effective at removing grain sizes that damage coral tissues (Stewart et al. 2006). In temperate regions (northwestern Atlantic), the herbivorous crab Mithrax sculptus removes algae and invertebrates growing on or near the coral Oculina arbuscula and thus prevents algae from overgrowing and killing the host coral (Stachowicz and Hay 1999). Other subtle benefits to hosts are difficult to identify. The shrimp Ancylomenes yucatanicus excretes ammonia, which represents a source of bioavailable nitrogen to symbiotic zooxanthellae contained in the tissue of the host sea anemone Condyllactis gigantea (Spotte 1996). Whether other symbiotic crustaceans represent a potential source of regenerated nitrogen for other host species (e.g., sea anemones and corals harboring symbiotic zooxanthellae) remains to be addressed. These examples highlight the difficulties of establishing the costs and benefits experienced by symbiotic partners. Some symbiotic crustaceans appear to be clearly parasitic; for example, endosymbiotic copepods, tantulocarids, rhizocephalan cirripedes considering their aberrant form and the extremely negative effects experienced by their respective hosts. Potential benefits (e.g., increased growth rate) generated by these symbiotic crustaceans cannot out-balance the costs for hosts (e.g., permanent castration). In most cases, though, examining (and quantifying) the totality of the costs and benefits experienced by all partners of a symbiotic relationship is challenging. Characterization of these partnerships as parasitic, commensal, or mutualistic is often hard to sustain because little or no empirical information is available (characterizations in Table 7.1 are tentative for most cases). Many more studies examining the totality of the costs and benefits experienced by symbiotic partners, ideally measured in terms of fitness proxies (e.g., offspring production), are needed in order to better evaluate the evolution of these associations. Other than the more evident cases of parasitism, the associations between crabs in the genus Trapezia and scleractinian corals (e.g., Pocillopora and Acropora) are some of the few symbiotic relationships that have been well studied in terms of the costs and benefits experienced by all partners. Trapezia crabs were first considered to be parasites because of their feeding habit on coral tissue and mucus from polyps (Knudsen 1967, Stimson 1990). Although not formally quantified, the crab’s feeding behavior most likely represents a cost to their hosts in terms of fitness. However, crabs actively defend their colonies from predatory sea stars, remove mucus produced by other organisms that is deleterious to corals, and discard sediment and remove sand grains that damage colony tissues (Glynn 1980, Stewart et al. 2006, Stier et al. 2010). These activities imply that these same crabs provide considerable benefits to their coral hosts. The Trapezia–Pocillopora partnership is now considered to be mutualistic, with net benefits for both crabs and coral colonies (Stewart et  al. 2006, Stier et  al. 2010). Another putative example of a mutualistic symbiosis is that between the shrimp Alpheus cf. armatus and the sea anemone B.  annulata in the Caribbean (Smith 1977). Last, mutualistic interactions also include caridean “cleaner” shrimps that remove parasites from fish hosts (Limbaugh et al. 1961, Becker and



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Grutter 2004)  and shrimps in the genus Alpheus symbiotic with goby fishes (Karplus and Thompson 2011). Nonetheless, Alpheus shrimps do serve as hosts and provide shelter to fishes rather than being symbiotic guests.

LIFE CYCLE OF SYMBIOTIC CRUSTACEANS Matching their taxonomic diversity, the life cycle and the timing of establishment of the symbiotic partnership vary widely in symbiotic crustaceans. At one extreme, amphipods (e.g., Hyperiidea and Caprellidea: Cyamidae [whale-lice], among others), mysids (H. harpax), caridean eusocial shrimps (e.g., Synalpheus spp.), and a few brachyuran crabs (e.g., T. moserii) that exhibit direct or abbreviated development have a simple life cycle, with benthic juveniles recruiting directly into the host dwelling from parental brood chambers. These juveniles might remain on the same host for the rest of their life (e.g., Synalpheus regalis; Duffy et al. 2000) or might leave the parental dwelling momentarily in search of new hosts from the same or different species where they can reestablish themselves (Thiel 2003). At the other extreme, the most complex life cycles occur in parasitic copepods and rhizocephalan cirripedes. In between extremes, many symbiotic crustaceans with indirect development spend their early (larval) life in the pelagic environment. Once they have reached the first postlarval stage, these species actively search for and settle in/on hosts to establish a permanent or semipermanent association with their partners where they grow, mature, and reproduce. Many symbiotic partnerships involving decapod crustaceans fit the life cycle just depicted (e.g., caridean shrimps Lysmata spp.; porcelain crabs Polyonyx spp.; almost all brachyuran crab symbionts, including coral crabs in the genus Trapezia spp.; and pea crab in the genera Austinixa, Pinnixa, and Pinnaxodes, among many others). However, several other symbiotic crustaceans with indirect development deviate from this pattern. For instance, in the fish lice Argulus spp., the only genus in the Branchiura for which the life cycle is well studied, females leave their hosts and temporarily visit hard submerged surfaces to deposit their eggs. These eggs hatch into a first swimming larval stage well-equipped for dispersal, with setose antennae and mandibles and rudiments of the maxillules, maxillae, and first two pairs of swimming legs. The second larval instar is the first parasitic ontogenetic stage, and the setae on the antenna are replaced by strong claws at this time (Gresty et al. 1993, Møller et al. 2007). The successive larval stages appear to leave and find new hosts at intervals, and most morphological changes during larval development are gradual. An exception occurs between the fourth and fifth larval stage, when the maxillule experiences a metamorphosis, changing from a long limb with a powerful distal claw into a short but powerful circular sucker (Boxshall 2005). Various molts succeed each other until maturity is reached, and copulation usually appears to take place on the external surface of the hosts (Rushton-Mellor and Boxshall 1994, Pasternak et al. 2000). Another example of indirect development is that of cymothoid isopods. Parental females in this group release offspring from their brood pouches as a modified “manca” (also called a “pullus II” stage) that swims efficiently thanks to heavily setose pleopods. These larvae need to find a fish to take their first meal within 1–2 days; otherwise, they die (Lester 2005). This life cycle contrasts to that of free-living peracarids with direct development, where juveniles assume an adult lifestyle shortly after emerging from the female’s brood pouch (Thiel 2003). These examples highlight the fact that many symbiotic crustaceans exhibit free-living dispersive stages early during their ontogeny. However, the opposite holds true in several other groups. For instance, in gnathid isopods (Gnathiidae), adult specimens do not feed and are found in cavities available in mud banks, dead barnacles, coral colonies, or sponges. In turn, recently hatched unfed juveniles or “zuphea” stages are those that seek a fish host to which to attach and feed on their blood. Due to the volume of blood consumed, the body of the zuphea expands. At this point, the zuphea becomes a “praniza.” The praniza leaves the host, finds shelter in the benthos, digests its meal, and molts. After molt, the new

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Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles zuphea searches again for another host fish on which to feed. This cycle is repeated twice, until the third praniza finds a cavity in which to mature (Upton 1987a,b, Kensley and Schotte 1989, Lester 2005). The most complex life cycles occur in parasitic copepods and rhizocephalan cirripedes. Such life cycles involve one or two hosts and subtle or considerable changes in body morphology and modification of the life cycle relative to that of their closest free-living relatives. For instance, the life cycle of parasitic copepods is abbreviated compared to that of their free-living counterparts that exhibit six naupliar dispersive stages and five copepodid stages preceding the adult phase. In parasitic copepods, the naupliar stages are usually lecithotrophic, the first copepodid is the ontogenetic stage that, most commonly, establishes the symbiotic relationship, and symbiotic partnerships usually involve a single host (Boxshall 2005). However, there are remarkable exceptions and deviations from the basic life cycle depicted above. For instance, Lernaeocera branchialis (family Pennellidae) features a life cycle that involves two nauplius stages and two, instead of a single, host species. Adult postmetamorphosis females that live on whiting (Merlangius merlangus) produce eggs that take 13 or more days to hatch as a nauplius I larva that passes through a nauplius II larval stage before turning into infective copepodids. These nonfeeding copepodids attach to the gills of the flounder Platichthys flesus, where they pass through all their developmental stages (four additional copepodid stages) to adulthood and copulation in a minimum of 25 days (Whitfield et al. 1988, Brooker et al. 2007). A second remarkable example of a complex life cycle in symbiotic copepods is that of the Monstrilloidea, characterized by most larval and all but the last juvenile (copepodid) phases being endosymbiotic and by a free-swimming pelagic adult phase that does not feed (Suárez-Morales 2011). In this group, eggs attached externally to the body of the parental females hatch into lecithotrophic nauplii that locate, attach, and burrow into the tissue of a mollusk or polychaete host. Once in the hemolymph of the hosts, the infective naupliar stage metamorphoses into an endoparasitic sac-like second naupliar stage that forms a protective sheath around its body but has two root-like processes for absorbing nourishment from the host. Development and transition among ontogenetic phases takes place within the host. Hosts are abandoned at the copepodid stage that, after a single molt, becomes a free-living adult, lacking all cephalic appendages other than the antennules (Huy et al. 2007, Suárez-Morales 2011). Epicaridean isopods (bopyrids, dajids, entoniscids, and cryptoniscids) are also recognized because of their complex life cycles. All known life cycles in this clade involve two crustacean hosts (Williams and Boyko 2012). For instance, in the bopyrid Orthione griffenis, symbiotic with the mud shrimp Upogebia pugettensis in the northeastern Pacific, parental females brood eggs in their brood pouch. These eggs develop and are released as a nonfeeding “epicaridium” larva that swims efficiently and seeks a copepod (usually a calanoid) host. The epicaridium attach to the copepod, perforate the exoskeleton, and feed on this intermediate host with the aid of its clawed pereopods and styliform suctorial mouthparts. Within days, the epicaridium metamorphoses into a “microniscus” larva that remains attached to the intermediate host, grows considerably, and metamorphoses into a cryptoniscus larva that leaves this intermediate host and swims until finding its second and definitive host (U. pugettensis). In this second, terminal host, the cryptoniscus metamorphoses into the first juvenile stage or bopyridium. In O. griffenis, the first bopyridium that parasitizes a host becomes a female, and subsequent isopods become males and live on the female (Williams and An 2009; Fig. 7.6). Thus, the life cycle of O. griffenis includes environmental sex determination, which has also been suggested for other bopyrids (Reinhard 1949). However, the sex in most other epicarideans is genetically determined (Williams and Boyko 2012). The life cycle of dasids, entoniscids, and cryptoniscids is not as well known as that of bopyrids. The Rhizocephala also have a remarkably complex life cycle. An example is that of Loxothylacus panopaei, symbiotic with the brachyuran crab Rhithropanopeus harrisii in the northwestern Atlantic (Glenner 2001). In this species, free-swimming male and female nauplius larvae are released from



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C Microniscus larva

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Infectious pelagic larvae Epicaridium larva

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Fig. 7.6. Epicaridean life cycle for the bopyrid isopod Orthione griffenis. A sexually mature female and male in the gill chamber of the gebiid mud shrimp definitive host (Upogebia pugettensis). The female releases epicaridium larvae that parasitize calanoid copepod intermediate hosts. The epicaridium larva metamorphoses into a microniscus larva and then a cryptoniscus larva that settles onto a definitive mud shrimp host. The first juvenile isopod (bopyridium) to parasitize a host becomes female; subsequent isopods become male(s) and live on the female. Scale bar: 1 cm for definitive host (rest not to scale). From Williams and Boyko 2012, courtesy of the Creative Commons Attribution License, and Williams and An (2009), with permission from Oxford University Press.

the parental externa. The nauplii develop into cyprids after 2 days. The male cyprid detects and settles at the mantle opening of a recently emerged externa on another host and metamorphoses into a dwarf male (a trichogon) that migrates through the mantle cavity and becomes inserted into one of the two receptacles of the virgin externa. Here, it will shed its cuticle, become established, and begin spermatogenesis. The externa will mature and begin to produce larvae only when a dwarf male has become established. In turn, female cyprids locate uninfested host crabs and settle on the gill lamella in the branchial chamber. Underneath the carapace of the cyprid, a kentrogon stage develop, which uses a cuticular-reinforced stylet to penetrate the integument of the gills to inject a “vermigon” into the open, blood-filled space of the gill lamella. The vermigon starts developing a rootlet branching system 10–12 days after injection into the host, and, after another month, the parasite finally protrudes a virgin externa through the integument of the host at the ventral part of the abdomen (Glenner 2001; Fig. 7.7).

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Fig. 7.7. The life cycle of the rhizocephalan cirripede Loxothylacus panopaei, from Glenner (2001), with permission from John Wiley and Sons. Solid lines illustrate developmental changes; dashed lines represent migration. (A) The externa (ex) underneath the abdomen of the host Rhithropanopeus harrisii. (B)  The externa releases free-swimming male and female nauplius larvae. After 2 days, the nauplius larvae develop into cyprids. (C) The male cyprids detect and settle at the mantle opening of a recently emerged externa (I). The settled cyprid metamorphoses into a dwarf male, which becomes inserted into one of the two receptacles of the virgin externa. (D) Female cyprid locates host crabs and settles on the gill lamella (D1) in the branchial chamber. (E) A kentrogon (ken) develops underneath the carapace of the cyprid. hcu, cuticle of the gills; cc, carapace of the cyprid. (F) The cuticular-reinforced stylet penetrates the integument of the gills and injects a vermigon into the open blood-filled space of the gill lamella. Abbreviations: st, stylet; vg, vermigon. (F1) A median section of the vermigon in the area of the ovary anlage. Four cell types are represented: the a and b cells of the ovary anlage (ac, bc), the central core cells (ccc), and the cells of the epidermis. (G) Rootlet (branching) of an internal parasite 10–12 days after having been injected into the host. (G1) Median section of the rootlet (rl) in the area of the ovary anlage. The primordial mantle cavity (amc) has already developed. (H) After about a month, the virgin externa (ex) can be seen through the integument of the host at the ventral part of the abdomen. (H1) Vertical section though the virgin externa of H. The externa is about to erupt through the cuticle of the host. Abbreviations: amc, mantle cavity; ov, ovary; cch, cuticle of the host. (I) The recently emerged externa on the abdomen of the host. To continue its development, the virgin externa has to receive at least one dwarf male in one of its two receptacles. (I1) A vertical section through the externa as depicted in I. A cyprid has settled at the opening to the mantle cavity. A dwarf male (a trichogon) will develop underneath the carapace of the cyprid and migrate through the mantle cavity to the opening of one of the two receptacles. Here, it will shed its cuticle, become established, and begin spermatogenesis. (J) Having received dwarf males, the externa (ex) will now mature and begin to produce larvae.



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Last, the Tantulocarida deserve to be mentioned, considering their exceptional life cycle, which includes a rare sexual and a common asexual (parthenogenetic) phase. Asexual females produce a tantulus larva with a well-defined cephalothorax and trunk (Fig. 7.8A,B). This larva spends time in the benthos seeking a suitable host (a peracarid, copepod, or ostracod) to which it attaches with an oral stylet that punctures the host’s cuticle. The larva sheds its trunk and develops into a new asexual (parthenogenetic) female without mating (Boxshall and Lincoln 1987; Fig. 7.8C). The new trunk of this female expands to accommodate the growing asexual larvae until they are released. In turn, during the sexual phase, the tantulus larva attaches to the host but does not shed the trunk. Instead, a sac-like expansion forms on the larval trunk from which sexual adult males or females develop. Once adults attain sexual maturity, the walls of the sac-like expansion rupture, releasing these adults to the external environment. The remaining portion of the sexual cycle is not well known. However, sexual dimorphism is pronounced in this group; males exhibit well-developed swimming appendages and paired clusters of chemosensory aesthetascs

Fig. 7.8. Life stages in the Tantulocarida. (A) Tantulus larva of Itoitantulus misophricola in lateral view. From Huys et al. (1992), with permission from Zoological Science. (B) Live tantulus larva of Arcticotantulus kristenseni attached dorsally to an harpacticoid copepod host. From Knudsen et al. (2009), with permission from Magnolia Press. (C) Parthenogenetic female of A. kristenseni with embryos inside. Arrow points at the head of the female. From Knudsen et al. (2009), with permission from Magnolia Press. (D) Male in late stage of development of A. kristenseni attached to cephalon of an harpacticoid copepod. Cephalic stylet in the larval head (cs) and male antennular aesthetascs (aes) are indicated. From Knudsen et al. (2009), with permission from Magnolia Press. Scale bars: A = 20 micrometers; B = 50 micrometers; C and D = 100 micrometers.

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Crustaceans as Symbionts: An Overview of Their Diversity, Host Use, and Lifestyles (Fig. 7.8D). Thus, it is believed that the males actively search for receptive females. Once females are found, males presumably inseminate them using a well developed penis-like intromittent abdominal organ via a mid-ventral copulatory pore. The fertilized eggs develop within the expandable cephalothorax of the sexual females until ready to hatch as a fully formed tantulus or other larva (Boxshall and Lincoln 1987, Huys et al. 1993). Once symbiotic partnerships have been established, various symbiotic crustaceans appear to be territorial, protecting “their” host individuals against conspecific (or even heterospecifics) via agonistic interactions. Nonetheless, formal experimental studies demonstrating territorial behavior have been conducted in only a few species of the Decapoda that dwell on their hosts either solitarily or as reproductive pairs (Baeza 2010). Whether or not highly modified symbiotic crustaceans (e.g., endosymbiotic rhizocephalans and epicaridean isopods) display territorial behaviors remains to be addressed.

COMPARISON WITH OTHER INVERTEBRATE GROUPS AND FUTURE DIRECTIONS Symbiosis is common in marine invertebrates. Sponges, cnidarians, ctenophorans, flatworms, nemertean, nematodes, priapulids, echiurid, annelids, mollusks, equinoderms, and tunicates, among others, have been reported to engage in symbiotic associations with other marine vertebrates or invertebrates (Vermeij 1983, Margulis and Fester 1991). Importantly, most of the clades just mentioned are used as hosts by other invertebrates rather than being themselves the symbiotic guests of other organisms. Even so, there are several remarkable groups of invertebrates that do use other organisms as hosts. For instance, in the Porifera, boring sponges are capable of excavating complex galleries in corals (e.g., Cliona spp.). In the Cnidaria, various representatives of the subclass Hexacorallia, order Zoanthidea are epizootic on sponges (e.g., Zoanthus spp.). Three classes of flatworms (Platyhelminthes) are exclusively parasitic (Cestoda, Monogenea and Trematoda) and exhibit complex life cycles. These parasites exhibit considerable body modifications during their life and use one, two, or three hosts to complete their life cycle. Other symbiotic invertebrates include nemerteans parasitic on the egg masses of decapod crustaceans (e.g., Carcinonemertes spp.), the enigmatic Symbion pandora (Phylum Cycliophora) living on the mouthparts of lobsters, and aberrant polychaetes in the order Myzostomida that are endosymbiotic with echinoderms. Still, none of these particular monophyletic clades displays the wide diversity, in terms of morphology, feeding strategies, and life cycles, herein shown to occur in symbiotic crustaceans. In crustaceans, members from almost all major taxonomic groups have established symbiotic relationships with other marine invertebrates, especially sessile invertebrates. Furthermore, a few crustaceans have established symbiotic partnerships with most unusual partners, including jellyfish, horseshoe crabs, amphibians, reptiles, birds, and mammals. Still others are parasites of humans (Tappe and Büttner 2009). This review demonstrates that the adoption of a symbiotic lifestyle represents a major environmental adaptation in crustaceans. Many groups of crustaceans not included in this review do serve as hosts and provide shelter to other organisms that, in turn, might benefit them (e.g., caridean shrimps in the genus Alpheus symbiotic with goby fishes, Karplus and Thompson 2011; anomuran crabs harboring sea anemones on “their” shells, Ross 1983; brachyuran crabs masking their bodies with sponges, Guinot et al. 1995). These symbiotic partnerships, in which crustacean act as hosts rather than as symbiotic guests, are not uncommon. This information underscores the fact that the symbiotic lifestyle in decapod crustaceans is even more recurrent than shown in this review. The ecology of crustaceans providing shelter to other marine organisms deserves further attention.



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Although the symbiotic lifestyle is pervasive in crustaceans, the incidence of symbiotic partnerships varied among taxonomic groups and was low or null in various clades (e.g., Remipedia, Cephalocarida, Branchiopoda, Cumacea, and Tanaidacea, among others). Various groups in which symbiosis is unusual live in freshwater or have an almost entirely pelagic life cycle. Other groups inhabit deep-sea environments. These habitats, with fewer life forms and less predictable and persistent productivity, might provide crustaceans with few evolutionary opportunities to exploit potential hosts. Yet symbiotic lifestyles cannot be discarded and remain plausible in these environments considering how little we know about their diversity. Many groups of crustaceans in which symbiosis is the exclusive or predominant lifestyle are species-rich. For instance, in the Decapoda, examples include crabs from the superfamily Pinnotheroidea (302 species) and the superfamily Trapezioidea (56 species) and shrimps from the subfamily Pontoniinae (562 species). In many cases, the diversity of these symbiotic groups is considerably higher than that of their closest free-living relatives. For instance, in decapod caridean shrimps pertaining to the family Palaemonidae, symbiotic shrimps from the subfamily Pontoniinae are more diverse than those pertaining to the predominantly free-living sister family Palaemoninae (562 vs. 372 species, respectively; De Grave 1999). This comparison begs the question as to whether or not the symbiotic lifestyle represents a key innovation favoring adaptive radiations in crustaceans. The adoption of a symbiotic lifestyle is believed to favor adaptive radiations in other groups of marine vertebrates such as shrimp-associated gobies (Thacker et al. 2011), sponge-dwelling gobies (Herler et al. 2009), and other coral-associated fish (Ruber et al. 2003). Studies on the phylogeny and life history of monophyletic clades of crustaceans containing both free-living and symbiotic species is warranted because it will test whether the adoption of a symbiotic lifestyle drives speciation and/or extinction rates (Fransen 2002).

CONCLUSIONS In summary, symbiotic crustaceans represent a very interesting model group for ecological, behavioral, and evolutionary studies. More detailed ecological studies on several species of ecto- and endosymbiotic crustaceans are needed to evaluate their adaptations and interactions with their respective hosts. Molecular phylogenetic analyses are also needed to conclude about the effect of the symbiotic lifestyle on body, coloration, and color pattern modification. Furthermore, robust and comprehensive phylogenies of several groups may be used to propose and test hypotheses about the evolution of social systems and symbiotic interactions in the marine environment. Last, comparative studies including several species of symbiotic crustaceans are needed to better understand the diversification processes in this interesting clade of symbiotic organisms in particular and in marine invertebrates in general.

ACKNOWLEDGMENTS This is Smithsonian Marine Station at Fort Pierce contribution number 972. I sincerely appreciate the comments of editors that improved previous versions of this manuscript.

REFERENCES Adlard, R.D., and R.J.G. Lester. 1994. Dynamics of the interaction between the parasitic isopod, Anilocra pomacentri, and the coral reef fish, Chromis nitida. Parasitology 109:311–324. Baeza, J.A. 2010. The symbiotic lifestyle and its evolutionary consequences: social monogamy and sex allocation in the hermaphroditic shrimp Lysmata pederseni. Naturwissenschaften 97:729–741.

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8 PREDATOR ADAPTATIONS OF DECAPODS

Kari L. Lavalli and Ehud Spanier

Abstract Mobile, surface-dwelling decapods (reptantians and some macrurans) roam across all benthic substrates (e.g., algal surfaces, rock substrates, corals, and soft bottom) in search of food and mates, to find thermal regimes beneficial to egg and larval development, to locate circulation patterns conducive to distributing larvae to settlement habitats, or to escape near-shore wave action in various seasons. This mobile existence leaves them exposed to a variety of predators that are both diurnally and nocturnally active. Since predation affects the fitness of individuals in a prey population, it is an important selective force that has caused modifications in the morphology, physiology, chemistry, life history, and behavior of benthic decapods. As a result, decapods have evolved a variety of antipredator tactics including predator avoidance mechanisms, in which the predator is avoided altogether, and antipredator mechanisms, in which prey act to avoid attacks or survive after an encounter by actively engaging in behaviors that foil attacks. This chapter illustrates the various methods used by benthic reptantian and macruran decapods to escape predation while engaging in activities necessary for survival of both individual and species.

INTRODUCTION Decapods have a long evolutionary history that dates back to the Paleozoic with several radiations events occurring thereafter (Feldmann 2003). The first of these events occurred in the Triassic with the emergence of numerous macrurous forms, and this was followed by an expansion of brachyuran forms in the Cretaceous, with subsequent radiation into modern forms in the Eocene (Schram 1986). High latitudes seemed to have served as hot-spots of decapod origins (many primitive forms) with lower latitudes giving rise to more derived forms (Feldmann 2003). Most benthic decapods today have complex life histories that involve some period of time as free-living, oceanic

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larvae followed by a settling stage (the postlarvae, known by a variety of terms such as megalopae, nistos, pueruli, etc.) that brings the individual to the benthos. Benthic decapods inhabit a variety of coastal, estuarine, lagoon, and deep-water habitats in all seas with very few in the polar regions (García Raso et al. 2008). They live in depths ranging from 0 m (intertidal) to thousands of meters (caridean shrimp have been noted at 6,000 to nearly 7,000 m in the hadal zone; Jamieson et al. 2009), thereby encountering habitats that vary greatly in structure. Shallow-water species encounter vegetated, rocky (pebbles, cobbles, boulder), shelly, or reef substrates (living and rubble), and, even within such substrata, patchiness of structure might be common such that refuges can be in short supply (Wieters et al. 2009), leading to competition both between conspecifics and amongst species. Some species found in either shallow or deeper waters are capable of dwelling in soft, featureless, bottom substrata into which they can either dig or bury (Faulkes 2013), but even these may provide hiding structures via other living organisms such as sponges or sea pens. Benthic decapods exhibit a wide range of movement patterns for a variety of purposes including spawning, brooding of eggs at temperatures advantageous to larval development, release of larvae, foraging, relocating of home ranges or home shelters, locating and acquiring mates, avoiding suboptimal conditions (extreme temperatures, changes in salinity, turbulence and wave action), and migration (Pittman and McAlpine 2001). Movement patterns may change over the life history of the species (so-called ontogenetic shifts) such that habitats suitable for recent benthic recruits and young-of-the-year (i.e., nursery grounds) may differ greatly from those suitable for older juveniles, subadults, and/or adults. For these decapods, a series of interlinked habitat types is necessary to meet the changing requirements in both food and shelter that occur during the life history stages of an individual (Acosta et al. 1997). Thus, ontogenetic stages of benthic decapods may develop stage-specific antipredator tactics or may shift from primarily using avoidance mechanisms to using antipredator mechanisms as they become large enough to fend off attacks. In contrast, some of the smaller species of benthic decapods may settle into coral heads, sponges, or anemones from which they never emerge (“obligate symbionts”), whereas others may display site fidelity around a home range where they engage in routine life activities, such as feeding, resting, and maintaining and defending their shelter. Such home ranges may expand or contract in size with the seasons or with the tides (Pittman and McAlpine 2001). Some benthic decapods may engage in long migratory movements (as per Herrnkind 1980) that usually move the animal offshore in specific seasons and bring it back inshore at other seasons in an attempt to create a more stable thermal or wave regime that could enhance growth or larval development. These movement patterns have the potential of exposing the animal to a variety of predators, each of which may vary in predatory tactics. Hence, we see benthic decapods employing multiple strategies to counter predation with the ability to shift from one strategy to another or to combine strategies when necessary. Predators vary according to the habitats and depths at which benthic decapods live. Shallow-water species may be subject to predation by fish, some cephalopods, other decapods, and birds. Typically, decapods that use intertidal habitats where food may be more plentiful might entirely avoid fish and cephalopod predators only to face a higher predation rate by birds or other terrestrial forms. By shifting to subtidal habitats, those same decapods may avoid bird predation only to face more fish, decapods, or cephalopod predation; however, the rate at which predation occurs typically decreases with depth (Krediet and Donahue 2009)  because marine organisms generally have lower metabolic rates than birds and other terrestrial vertebrates. Species found on continental shelves and slopes are typically subject to a larger variety of fish predators, as well as mammals, cephalopods, and other decapods, including conspecifics (Martins 1985, Howard 1988, Dunham et al. 2005). Therefore, different mechanisms for avoiding predation will result from differing risks of predation and the different modes of predatory attack. Natural mortality estimates have been made for various commercially fished species and suggest higher predation rates on new benthic recruits and juveniles than on adults. For example, estimates

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Predator Adaptations of Decapods for spiny lobster (Palinurus sp.) suggest a fairly low predation rate of adults with a life span of 15–30 years (Pollock and Melville-Smith 1993, Groeneveld 2000, Groeneveld et al. 2006). The mortality rates of young juveniles, however, are thought to be extremely high (80–96%; Herrnkind and Butler 1994, Phillips et al. 2003). Natural mortality rates for snow crabs (Chionoecetes sp.) and king crab (Lithodes and Paralithodes sp.) are thought to be relatively low (18–26%), based on estimates for the instantaneous mortality (M = 0.3–0.2; Siddeek et al. 2002). In contrast, mortality rates for adult blue crabs (Callinectes sapidus) and mud crabs (Scylla olivacea and Scylla serrata) are thought to be approximately 50–63% per year, based on M values of 0.42–1 (Hill 1975, Moser et al. 2005, Hewitt et al. 2007), but for other species (e.g., Portunus sanguinolentus), natural mortality may be nearly 83% (Lee and Hsu 2003; but see also Kitada and Shiota 1990 who argue that natural mortality in another portunid, Portunus trituberculatus, is low). Adult benthic shrimp (Pandalus hypsinotus) may also have high natural mortality rates, with some estimates reaching as high as 86% (M = 2; Dunham et al. 2005). For crab species that move with the tide from the subtidal to lower intertidal, or even for those that can live semiterrestrially, predation by birds may be extremely high. Gulls are estimated to remove 30–50% of the Cancer borealis crabs that are accessible on the shoreline during low tide and even down to 1 m water depth (Ellis et al. 2005). Mortality can be extremely high on shoreline crabs, as demonstrated by tethering experiments in which 95% were killed by gull predators at 0 m, although mortality decreased 3.5-fold at depths of 2 m (Krediet and Donahue 2009). Despite a dearth of data on mortality rates of most decapods, it is clear that predation represents a significant problem with which decapods must deal throughout their life, and one that greatly influences all aspects of their lifestyle. As a result, decapods have evolved predator avoidance tactics for the purpose of avoiding predator encounters and/or detection and antipredator tactics for the purposes of avoiding consumption once a predator has encountered them. Typical predator sequences involve a sequence of events, and, as a predator is able to move further down the sequence by countering defenses, consumption becomes more and more likely. This sequence of events (as per Endler 1991) includes (i) the Encounter, in which the predator comes close enough to prey to detect it; (ii) Detection, in which the predator is able to distinguish the prey from its background; (iii) Identification, in which the predator determines that the prey is both profitable and edible and makes the decision to attack; (iv) the Approach and Attack; (v) the Subjugation, in which the predator prevents the escape of the prey; and (vi) Consumption. Most decapod taxa use a combination of tactics and differ only by the extent to which avoidance is favored over the use of antipredator tactics.

PREDATOR AVOIDANCE MECHANISMS The most ubiquitous and arguably the primary predator avoidance mechanism of any benthic decapod is sheltering by means of being withdrawn or wedged into a crevice, hidden among masking vegetation, or buried into substrate (Faulkes 2013). However, decapods have also evolved a number of other strategies and mechanisms that effectively reduce the likelihood that they will ever be encountered. These include shifts in activity patterns, being dispersed in such a way as to appear rare, using polymorphic coloration patterns or camouflage to avoid detection, death feigning, or masquerading as something else. Typically, more than one of these avoidance mechanisms is used at a time so that responses to a variety of situations and predators can be made in an appropriate fashion. Reduction of Encounter Rates The simplest way of limiting predatory encounters is to avoid exposure to predators by making oneself rare. This can be accomplished by occupying a different microhabitat from the predator and simultaneously shifting activity levels to a period during the day or night when major



Kari L. Lavalli and Ehud Spanier

predators are not active. Clear circadian rhythms have been recorded for a variety of decapods including clawed, spiny, and slipper lobsters (Kanciruk and Herrnkind 1973, Smith et al. 1998, Jury et al. 2005); portunid crabs (Ryer 1987, Abelló et al. 1991); cancrid crabs (Chatterton and Williams 1994, McGaw 2005); squat lobsters (Warman 1990); and shrimps (Heegaard 1967, Rasheed and Bull 1992, Burrows et al. 1994). Typically activity patterns are entrained to crepuscular periods or tidal cycles (Fig. 8.1A–D). In some cases, adult behavioral patterns may differ from those displayed by juveniles due to differences in vulnerability to predators. For example, juveniles of nocturnal species may be less active at the crepuscular periods than adults, and they may increase their activity with the nocturnal period but only engage in short-distance foraging bouts from their shelters, returning to their shelter numerous times rather than engaging in long-distance, long-duration foraging bouts (Spanier et al. 1998, Weiss et al. 2008). However, if there is a transition period between the activity levels of diurnal fishes and nocturnal fishes such that the predator population actually increases during crepuscular periods, then those species that emerge at dusk or dawn may actually suffer higher predation rates regardless of their ontogenetic stage (Oliver et al. 2005). Where do benthic decapods hide when not active and out in the open? Again, taxa are highly diverse in the ready-made structures they can use, the shelters they can create, or the substrates they can manipulate to effectively “disappear.” For those species that live on less structured substrates, a rapid burying behavior effectively hides them beneath the sediment surface and seems to serve as a predator avoidance mechanism (Nye 1974, Barshaw and Able 1990; Fig. 8.2A,B). Nine families of brachyuran crabs (Atelecyclidae, Calappidae, Cancridae, Corystidae, Hymenosomatidae, Leucosiidae, Matutidae, Mictyridae, Portunidae, and Raninidae; Bellwood 2002, Takeda and Murai 2004, McGaw 2005), a variety of sand crabs (hippids and albuneids; Faulkes and Paul 1997), several species of penaeid shrimp (Moller and Jones 1975, Primavera 1997, Freire et al. 2011), and some slipper lobsters (Faulkes 2006) are known to rapidly bury themselves in soft substrata. Appendage use for burial differs amongst taxa and is reviewed by Faulkes (2013). Depth of burial seems dependent on both substratum and taxon, such that a species that can bury deeply in one type of substratum may only be able to effect a shallow burial in another substratum (cf., Barshaw and Able 1990). Generally speaking, the entire animal is buried with only an exhalant current or eyestalks indicating its presence (Fig. 8.2A), although apparently a few species can completely bury without any direct connection to the surface (Bellwood 2002). Burial can be for short periods of concealment in some species, but, in others, burial may occupy most of the daily cycle until the animal forages for food (Nye 1974, Abelló et al. 1991, McGaw 2005). Seasons can affect length of time buried, with some species remaining buried for up to 2 weeks in winter months (cf., Cancer magister; McGaw 2005). Most decapods can effect burial quite rapidly with measured times ranging from a few seconds to several minutes, and, generally speaking, the time to bury is positively related to size (McGaw 2005, Faulkes 2006, Anker 2010). Some taxa are well adapted for digging and can actively manipulate the substrate to dig a den or a burrow or to improve an existing structure (Fig. 8.2C,D,E). Aside from lobsters and a variety of prawns and shrimp, representatives of eight families of brachyurans are also known to burrow (Beliidae, Gecarcinidae, Goneplacidae, Grapsidae, Mictyridae, Ocypodidae, Portunidae, and the Potamoidea; Bellwood 2002). However, the act of creating a burrow within a variety of substrata does not necessarily mean that all substrates are equally protective against predators, and success may depend largely on the ability of the predator to manipulate or disrupt the substratum and the complexity of the burrow constructed (Lavalli and Barshaw 1986, Laprise and Blaber 1992, Hovel and Lipcius 2002). For species living in complex habitats, a variety of structures exist that are ready-made and can be anything from other organisms (sea fans, corals, anemones, sponges, mussel beds, seaweed fronds, root systems of marine plants, etc.; Fig. 8.2D) to rock ledges and outcroppings, boulders, or cobble beds (Fig. 8.2E), or, finally, to man-made structures (ghost fishing

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Fig. 8.1. Activity patterns of various decapods. (A) Activity record of a single lobster, Homarus americanus, in an activity racetrack showing the typical nocturnal pattern in movement (thin line represents light; thick line illustrates activity). Modified from Jury et al. (2005), with permission from Elsevier. (B) Mean percent with 95% confidence intervals of movements by nine lobsters, Homarus gammarus, tracked for more than 2 weeks moving between reef units at different times of the day (black bars represent night, white bars indicate day, gray bars indicate sunset/sunrise). Modified from Smith et al. (1998), with permission from Springer. (C) Mean numbers per hour ([log10(1 + n)] transformed) of Carcinus maenas crabs moving beneath subtidal and intertidal cameras relative to the times of sunrise (SR) for observations under midnight and sunset (SS) for observations before midnight. Modified from Burrows et al. (1994), with permission from Elsevier. (D) Mean number of Pachygrapsus marmoratus crabs (+ SE) active during different light conditions (left panel) and different tidal phases. From Cannicci et al. (1999), with permission from Springer.



Kari L. Lavalli and Ehud Spanier

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Fig. 8.2. Various modes of sheltering by decapods. Burial by (A)  Ranina ranina (spanner) crab showing only eyes and antennules and (B) Thenus orientalis (slipper) lobster. Crevice used by (C) alpheid (Alpheus djeddensis) shrimp and associated goby, and (D) Palinurus argus (spiny) lobster under coral head. Sheltering in structures by (E) Homarus americanus (clawed) lobster and Cancer borealis (rock) crab in rocky artificial reef and (F) Scyllarides latus (slipper) lobster in artificial reef structures. A, B, and C, courtesy of Guido T. Poppe and Philippe Poppe: www.poppe-images.com; D, courtesy of Michael Childress; E, courtesy of MA Division of Marine Fisheries staff; and F, courtesy of Stephen Breitstein.

gear, sunken ships, and artificial reefs built from cars, buses, tires, or concrete structures; Fig. 8.2F). Numerous studies have demonstrated specific preferences for shelter dimensions, number of openings, and presence of conspecifics, but the presence of a predator influences these preferences by decreasing their importance (Eggleston and Lipcius 1992, Gristina et al. 2009). Predators can also influence the time spent within a shelter (Wahle 1992, Rossong et al. 2011). Predation mortality is substantially reduced for individuals in shelters versus on open or cryptic substrata, especially during the day and for small individuals (Fig. 8.3A,B,C). Because of the importance of shelter-providing habitat to survival, competition for shelters by sympatric species of decapods can be intense. Those species that display better resource-holding potentials for such shelters are likely to shift predation pressure to the species that they outcompete or are likely to cause lethal and sublethal effects for conspecifics of different age cohorts (Sainte-Marie and Lafrance 2002, Hulathduwa et al. 2011). Shallower waters with structural features that provide shelter can also enhance survivorship, particularly for the small juvenile stages of many decapods (Hines and Ruiz 1995). Survival is more varied in species that create their own burrows, especially if their predators can either disturb the substrate, move pebbles and rocks, or also dig and burrow after their prey (Seiple and Salmon 1982, Barshaw and Lavalli 1988, Wahle and Steneck 1992). Mortality is also decreased for species that are not necessarily sheltered or buried, but that use cover provided by seaweeds, seagrasses, drift algae, or other animals (penaeid shrimp; Coen et al. 1981, Wilson et al. 1990, Herrnkind et al. 1997a,b), and, in some species, survival is enhanced when cover is dense (Fig. 8.3D). Reduction of Detection via Crypsis and Camouflage If the availability of food resources, the need to mate, or a need for reduction in competition leads some benthic species to be active when their predators are also active, then a number of methods can be employed to make the task of detection more difficult. Camouflage is commonly employed and includes all forms of concealment that act to prevent both detection and recognition of prey

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Kari L. Lavalli and Ehud Spanier

(Stevens and Merilaita 2009). Hence it could involve (i) the passive use of colors or patterns that help the prey blend into the background (crypsis) combined with mimicry of rubble, rock, or other inedible objects by sculpturing of the carapace (concealment) or (ii) active decoration of the shell surface to blend in with background fauna or flora or to masquerade as something other than a decapod (Stevens and Merilaita 2009). In addition, disruptive coloration can make it difficult for a predator to determine a prey’s true shape and outline (Stevens and Merilaita 2009), thereby interfering with a predator’s search image. Because shell color is determined by the number and distribution of chromatophores and by the amount of astaxanthin (a carotenoid pigment) incorporated into the exoskeleton at molt, cryptic coloration is dependent upon the diet consumed by the different ontogenetic stages of decapods (Casariego et al. 2011). Thus, for species that settle into specific nursery habitats from which they migrate, as they grow and age, changes in coloration may accompany changes in diet that arise from the exploitation of different habitats and from maturation of their feeding apparatus. For example, some majoids can change the color of their carapace throughout their life span by sequestering pigments from algae that they specifically seek out to ingest (Hultgren and Stachowicz 2009); in the burrowing grapsid crab Neohelice granulata colors differ based on whether they are located in mudflats where they deposit-feed or in marsh habitats where they adopt a more herbivorous and detritivorous diet (Casariego et al. 2011). In contrast, Carcinus maenas and Xantho poressa juveniles are colored differently from adults when they settle and spend their juvenile stages in Mediterranean Posidonia oceanica meadows; adults live in stones (X. poressa) or soft bottoms (C. maenas) and have a more uniform coloration pattern that does not dramatically change from molt to molt (Bedini 2002). Cryptic coloration is well known for small crabs, both those that remain small throughout their life span (Bedini 2006), and those in early developmental stages (Palma and Steneck 2001, Manríquez et al. 2008, Krause-Nehring et al. 2010). Typically, these crabs exhibit different color morphotypes and settle into heterogenous substrates composed of shell hash or small rocks and pebbles. Sometimes within a single species, these morphotypes include specific color morphs and specific pattern morphs that can be combined to create a variety of polymorphisms (e.g., Cancer irroratus has six colors and five patterns that can create 30 morphotypes, Krause-Nehring et al. 2010). Both the size of the crabs and their variable coloration help them to blend into the background and make it difficult for predators to create an effective search image (Todd et al. 2009). Within the brachyurans, 29 species have been described as exhibiting developmental polymorphic crypsis coming from the following families: Xanthinae, Cancridae, Portunidae, Epialtidae (majoids), Menippidae (stone and giant crabs), Hymenosomatidae (majoids), Platyxanthidae (eriphioids), Pilumnidae (hairy crabs), Pilumnoididae, Pseudoziidae, Sesarmidae, Varunidae (grapsids), and Ocypodidae (ghost and fiddler crabs) (Todd et  al. 2009). Only a few species have been tested to determine if the polymorphic crypsis actually reduces predation rates, but, in those species (Cancer irroratus, Paraxanthus barbiger), survival was significantly greater in multicolored, textured substrates compared to bare substrates (Palma and Steneck 2001, Manríquez et al. 2008). Smaller decapods, such as benthic shrimp, may associate with vegetation or algal-encrusted rocks that provide a surface in which they can blend or hide; the best known examples of these species come from the families Palaemonidae, Gnathophyllidae, Pandalidae, Hippolytidae, Penaeidae, and Alpheidae (Anker 2010) (Fig. 8.4A,B,C). The colors of hippolytids (e.g., Hippolyte, Latreutes, Heptacarpus, Tozeuma spp.) that are associated with marine plants are matched to the blades or thali and obscure their detection when they cling to blades during the day. At night, these shrimp display a transparent blue or aquamarine color because the chromophores producing the coloration patterns retract in the absence of light (Bauer 1981). Other shrimp (e.g., Palaemonidae, Penaeidae) mimic background colors with a single band of color (Fig. 8.4D). Palaemonids and alpheids can also mimic coloration of commensals with which they might live (Fig. 8.4E). Some shrimp (e.g.,

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Crangonidae and Hippolytidae) may mimic nonliving items from the environment, such as sand, rock, or rubble, because their carapace is sculptured with tubercles and ridges (Anker 2010; Fig. 8.4F,G). A number of crab and shrimp species associate with other living organisms that display complex architecture (spines, branches, coral heads, etc.) in which they can hide (Anker 2010). Generally, the coloration of these crabs helps them to blend into their host. In shallower waters,



Kari L. Lavalli and Ehud Spanier

many species of crabs are colored to match vegetation (e.g., Carcinus maenas or Pugettia sp.) or coralline algae (e.g., Cancer borealis and C.  irroratus) or are sculptured to look like rocks (Fig. 8.4H,J,K). Finally, those decapods that employ disruptive coloration do so via brightly colored bands on legs or antennae that obscures the outline of the body or breaks it up so as to not appear as an edible piece of food (Wicksten 2010). Disruptive coloration may also provide flicker-fusion camouflage, in which the markings blur during motion to match the background in which the shrimp is found (Stevens and Merilaita 2009; Fig. 8.4L). Generally, in the deep sea, benthic crustaceans are uniformly colored (yellow to red), and, regardless of whether they match the coloration of the substrate or not, that substrate reflects bioluminescent light and makes it difficult for predators to detect objects ( Johnsen 2005). In some cases, however, there are benthic crustaceans that are bicolored (e.g., red and white galatheid crabs); these are generally associated with rubble rather than featureless sand or mud and differ in their blue-green reflectance patterns, with one color having a high reflectance and the other having a low reflectance ( Johnsen 2005). Even though these reflectance patterns may not provide crypsis, deep-sea predators generally have poor contrast sensitivity and may not be able to “see” such bicolored decapods ( Johnsen 2005). Caridean shrimp of the family Gnathophyllidae both mimic the colors of their echinoid hosts and can hold their claws perpendicular to look like urchin spines (Patton et  al. 1985). Despite both camouflage and cryptic behavior, these shrimp prefer to dwell on urchin species that engage in extensive covering behavior, even if those urchins provide a less well-matched background to the shrimp’s coloration. When dwelling on urchins that do not extensively cover, the shrimp are more likely to be found on the oral surface rather than the aboral surface; this suggests that the covering behavior of the urchin provides additional protection to the shrimp than simply the urchin spines alone or cryptic coloration (Macía and Robinson 2009). Some commensal shrimp (Pontoniinae) are able to not only hide among their host’s tissues, but also can grasp such tissues with their dactyls and pull the tissue over their body, presumably to provide cover and greater protection (Metapontonia fungiacola with scleractinian corals; Yamashiro 1999). Many alpheid shrimp associate with a number of other species, including anemones (Smith 1977), corals (Patton 1975), gobies (Karplus 1981), brittlestars (Marin et al. 2005), sponges, and mud crabs (Silliman et al. 2003) (Fig. 8.2C). These associations are often mutualistic, with the shrimp either defending the host, codefending against predators, warning against predators, or providing burrows for gobies; in return, the shrimp gain access to food sources, are provided with shelter, or are warned about predator approaches. Death Feigning (Immobility) Death feigning behavior (otherwise known as “tonic immobility,” “thanatosis,” or “freezing”) is known in many prey taxa including decapods, and is a form of deception that causes the predator to treat its prey as already dead or to fail to detect it altogether because of the lack of movement. Thus, immobility may cause the predator to pass by the prey, which increases that animal’s chance of escaping once the predator has moved out of detection range. Examples of death feigning are seen in solenocerid shrimp, which are highly sensitive to movement and/or sound; when such movement or sound is detected, the shrimp stiffens all body parts and plays dead (Heegaard 1967). Likewise, highly cryptic slipper lobsters freeze in response to passing predatory triggerfish and may thereby avoid proper identification and detection (Almog-Shtayer 1988, Barshaw et al. 2003). Death feigning in clawed lobsters was also described by Herrick (1895) and has been noted in blue crabs (Callinectes sapidus; O’Brien and Dunlap 1975), in mangrove crabs (Camptandrium sp.; Tan and Ng 1999), in majoid decorator crabs (Wicksten 1993), and in the hairy crab (Pilumnus vespertilio; Kyomo 2001).

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ANTIPREDATOR (DEFENSIVE) MECHANISMS If avoiding the predator is unsuccessful, benthic decapods use a variety of antipredatory defensive mechanisms that depend on the taxon, the circumstances, and the stage in the predation sequence. These include the use of commensal associations, masquerade, unpredictable movements, the development of heavy armor (via a thick shell) and/or weaponry, the use of clinging to prevent dislodgement from the substrate, the development of aposematic signals via coloration or sound production, use of limb autotomy to effect escape, escape maneuvers, evolution of increased sociality with the benefits that accrue via the dilution effect or collective defense, production of alarm cues to warn conspecifics, and the use of poisons or unpalatable tissues. Disrupting the Proper Identification by Predator Protection by Associating with Other Organisms Species of shrimp (caridean and stenopodid) and crabs (mainly porcelain) may be commensals on living sponges, gorgonians, corals, sea anemones, crinoids, tubeworms, starfish, urchins, and nudibranchs or may live among the spines of sea urchins (Wicksten 2010, Meireles and Mantelatto 2008, Goy 2010). Frequently, these shrimp or crabs are color-matched to the host species so that they blend in with its features, but, for many of these associations, the host has stinging cells or other features that deter predators from their tissues and possibly from the symbionts living among those tissues. Nevertheless, very few experiments confirming this hypothesis have been conducted. Huang et al. (2008) examined whether physical (spicule) or chemical properties of the tropical sponge Amphimedon viridis provided any level of protection for symbionts (inclusive of decapods) found within the sponge and found that both hydrophilic and lipophilic extracts within alginate pellets deterred predators of the symbionts. Hence, the symbionts were afforded protection by associating with such sponges. More studies examining the actual interactions among symbionts and their predators need to be conducted to elucidate the potential antipredator function of these associations and the mechanisms by which the antipredator response is effected. Active Forms of Masquerade Spider crabs (Majidae family) associate with other species by deliberately attaching to their carapace surface a variety of living organisms (typically algae, sponges, hydroids, and worm tubes) via dense patches of specialized hooked setae possessed only by spider crabs (Wicksten 1993; Fig. 8.5A). These crabs begin decorating shortly after settlement into the benthic environment (Wicksten 1993), can cover their carapace in a time scale of hours to one day (Hultgren and Stachowicz 2009, 2011), and continue to decorate until they reach maturity (Wicksten 1979, Berke and Woodin 2008) or until their size exceeds the gape width of predatory fish in their ecosystem (Stachowicz and Hay 1999). Some smaller species decorate throughout their entire life (Berke and Woodin 2008). Shifts in amount of decoration with size could be the result of higher cost-to-benefit ratios of the extra load of other living organisms (Berke and Woodin 2008); the trade-off between metabolic needs of extra weight versus those needed to produce larger, dimorphic claws in males (Berke and Woodin 2008); or the reduction in the density of hooked setae on the carapace of larger individuals (compare coverage in Fig. 8.5B,C and 8.5D; Hultgren and Stachowicz 2009). For species that decorate, field tethering studies demonstrate higher survival rates in decorated than nondecorated individuals; furthermore, the presence of a predator increases the amount of decorating that is displayed by individual crabs (Thanh et al. 2003).

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Fig. 8.5. Masquerading crabs. (A)  Specialized hook setae used to attach decorations. (B)  Rugettia richii decorating with red algae pieces, (C) Libinia dubia decorating with noxious brown seaweed (Dictyota menstrualis). (D) Loxorhynchus crispatus decoration. (E) Hyas sp. decorated in sponges. (F) The dorippid Paradorippe granulate holding the lamellibranch Macoma over its carapace with the dactyli of the fourth and fifth pereopods. (G) The ethusid Ethusa mascarone carrying a shell covered by a sea anemone with its fourth and fifth pereopod. (H) The calappid crab Hepatus epheliticus with a sea anemone (Calliactis tricolor) on its carapace. A–D, courtesy of John Stachowicz; E, courtesy of staff of MA Division of Marine Fisheries; F and G from Guinot et al. (1995), from The Raffles Bulletin of Zoology, National University of Singapore.

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Predator Adaptations of Decapods In addition to masquerading effects, the algal species used for decoration are often unpalatable to predatory fish because of chemical toxins (diterpene alcohols; see Hultgren and Stachowicz 2011 for a listing of majoid species exploiting these algal species). These noxious algal species decrease predation rates in field settings (Stachowicz and Hay 1999, Hultgren and Stachowicz 2009) and cause predatory fish and octopuses to release or spit out well-decorated crabs in laboratory settings (Wicksten 1993). Decorating with sponges and noxious bryozoans also appears to deter predators, and the use of anemones (Fig. 8.5H) with stinging nematocysts seems likely to reduce predatory attacks (Hultgren and Stachowicz 2011). Hence, it is likely that decorating has evolved as an antipredator mechanism, but its maintenance over the crab’s lifetime and its extent represents the interplay between predation rates and metabolic costs (Berke and Woodin 2008). Crabs in the subfamily Dorippinae are known to carry pieces of shell, valves of lamellibranchs, starfish, sea urchins, sponges, debris, mangrove leaves, and various bivalves (Fig. 8.5E,F,G). Those that carry shells often choose shells with anemones affixed. They hold these items with their fifth pereopods and typically place the item on their dorsal surface to conceal themselves temporarily when danger approaches (Guinot et al. 1995). No studies have yet examined the effects of this behavior on predation rates. Responses to Approach of Predator Protean (Unpredictable) Behavior Protean behavior can include intermittent locomotion patterns caused by changes in speed, duration, and direction, as well as changes in the mode of movement (e.g., from walking to swimming) or changes in the media where the animal is located (e.g., from water to air or vice versa; Driver and Humphries 1988). When decapods change from a walking mode of locomotion to a swimming mode in response to the presence of a predator, generally they engage in what is commonly known as an “escape” response. Such escape responses may also include body rolls to one side or another and abrupt changes in vertical positioning that create unpredictability for the predator (Arnott et al. 1998). Escape responses are used by many crustaceans as a major defense against predators. In a kinematic analysis of optimal avoidance and evasion techniques (escape response to an attack) for prey, Weihs and Webb (1984) suggested that the optimal evasion technique involved escape at a small angle (up to 20 degrees) from the heading directly away from the predator. Domenici et al. (2011a) stated that the two most important variables in escape success were the directionality (% responses directed away from the threat) and the escape trajectories measured as the angle relative to the threat. They found that although it was logical that prey would always turn away from the predator, studies in many species had indicated that these “away” responses occurred only 50–90% of the time. They suggested that the small proportion of “toward” responses might introduce some unpredictability and could be an adaptive characteristic of the escape system. Similarly, they argued that although the optimal escape trajectory could be modeled on the geometry of the predator–prey encounter, unpredictability in trajectories might be essential for preventing predators from learning the simplest escape patterns. Escape Responses Benthic decapods have a variety of locomotory modes (walking; swimming by swimmeret beating, tail-flipping, or uropod beating; and punting) that can be performed on or off the substrate to avoid predators (Davis 1969, Paul 1971, Martinez et al. 1998) and largely reflect the differences in proportions amongst the body parts (cephalothorax vs. pleon vs. telson). Shrimp (macrurans) and lobsters (macruran-like reptantians) typically are forward-walking taxa with elongated pleons that



Kari L. Lavalli and Ehud Spanier

are exposed to potential attack. In contrast, crabs (reptantians) are forward- or sideways-walking taxa that have diminished pleons tucked under their wider-than-longer cephalothorax. Given these differences in body structure and locomotion, escape behaviors and strategies differ among decapods. A large, elongated pleon permits rapid flexions (tail flips) that can effectively propel the animal upward or backward to engage in escape swimming. Macrurans and macruran-like forms employ a rapid abdominal flexion, the direction of which depends on the location of the predatory stimulus and the axonal elements stimulated. Hence, attacks to the anterior carapace, rostrum, or antennae or strong visual stimuli excite the medial giant axons that innervate all abdominal segments and result in a reflexive flexion that propels the animal directly backward (Olson and Krasne 1981). Attacks aimed at the abdomen excite the lateral giant axons that innervate only the first three abdominal segments, and this excitation results in an upward somersaulting movement as half the abdomen flexes and half stays straight like a paddle (Wine and Krasne 1972). After this initial action, there are typically one or two pitching flips that turn the animal upside down, followed by several twisting flips that right the animal; subsequent swimming movements are produced by the non-giant axons that are excited after such escape tail flips are effected (Fig. 8.6A). Tail-flip responses have been well studied in the shrimp (Pandalus danae, Daniel and Meyhöfer 1989; Crangon crangon, Arnott et al. 1998, 1999), crayfish (Wine and Krasne 1972), and lobsters from all major families ( Jacklyn and Ritz 1986, Spanier et al. 1991, Newland et al. 1992); these responses are reviewed by Boudrias (2013). Shrimp typically “jack-knife” first (Fig. 8.6B), propelling themselves upward in the water column while rolling. Subsequent tail flips propel the animals straight backward, while swimming on their side (Arnott et al. 1998). Compared to shrimp, the more heavily calcified lobsters vary in the location of their center of mass depending on the size and weight of their anterior appendages (either claws or antennae). Thus, more thrust must be generated to maintain height above the substrate ( Jacklyn and Ritz 1986). As a result, for clawed lobsters and, to some extent, spiny lobsters with their large and long antennae, escape movements may be energetically costly and limited in their extent. Roll movements and righting reactions are brought about by rotation of the abdomen relative to the cephalothorax and asymmetrical movements of the pleopods (Cattaert et al. 1988). In contrast, scyllarid lobsters are heavily calcified but lack large and heavy anterior appendages and instead possess an expanded head fan in the form of their modified second antennae. Their center of mass is closer to the abdomen than it is in nephropids or palinurids. For these lobsters, large amplitude movements of the abdomen (“tail flexions”) drive the lobster quickly backward (acceleration) and are followed by powerless gliding (deceleration) as the abdomen straightens out ( Jacklyn and Ritz 1986, Spanier et al. 1991; Fig. 8.6C). A number of studies examining tail-flip swimming show that rates range from less than 1 to more than 25 body lengths per second (0.01–3 m/s) in various shrimp (Daniel and Meyhöfer 1989, Arnott et al. 1998, Yu et al. 2009), to 1–3 body lengths per second (~1 m/s) in slipper lobsters (Spanier et al. 1991), 0.065–0.5 m/s in clawed lobsters (Newland et al. 1988, Cromarty et al. 1991), and 0.4–28.9 body lengths per second (0.022–1.6 m/s) in spiny lobsters (Naeun and Shadwick 1999). These rates are similar to swimming rates of some predators (Arnott et al. 1998) and thus it is not clear how effective such tail-flip maneuvers are for escaping predation. For crayfish under attack, tail flips provide escapes rates ranging from 44% to 50%, whereas burst-and-coast swimming only provides a 20% escape rate (Herberholz et al. 2004); as yet, no one has examined escape rates in marine decapods. In species that have no terminal molt and continue to grow large in size, the effectiveness of the escape tail flip should diminish as the carapace enlarges and becomes heavier. Likewise, if the animal bears chelae (and/or long antennae), increasing size with growth will decrease the effectiveness of abdominal flexion as these appendages shift the center of gravity further forward (Vidal-Gadea et al. 2008) and increase drag. Some argue that increased chela size may be a compensatory mechanism for loss of effective escape swimming in large lobster-like species (Vidal-Gadea et al. 2008),

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Fig. 8.6. Escape maneuvers by (A) clawed lobsters showing the body movements when the lobster is tapped on the abdomen (left) or the anterior carapace (right). (B) Shrimp trajectories showing their initial jack-knife tail flip following by abdominal swimming. (C) Mediterranean slipper lobster Scyllarides latus showing their swimming trajectory from above (top) and the side (below). A, redrawn by Rachel Pollak from Wine and Krasne (1972); B, from Arnott et al. (1998), with permission from Journal of Experimental Biology; and C, from Spanier et al. (1991), obtained with permission from Elsevier.

but chelae have been shown to be ineffective weapons against fish and octopus and can be damaged either directly—rendered ineffective by damage to the meral joint—or become useless if eyestalks are removed and the weapon cannot be “aimed” appropriately (Barshaw et  al. 2003, Lavalli and Spanier 2001, personal observations). It is more likely that thickening the cuticle with successive molts (Pütz and Buchholz 1991), which adds strength to the carapace, may be a much more effective compensation for loss of the escape response (Barshaw et al. 2003), but the relationship between tail-flip capabilities, armor, and weaponry needs to be better studied. Reptantian crabs do not rely on tail flips for escape because their abdomens (pleons) are reduced in size and are tucked under the cephalothorax. As a result, they are not limited to a forward-walking



Kari L. Lavalli and Ehud Spanier

direction and can walk in any direction because the abdomen does not obstruct the movement pathway or add drag (Vidal-Gadea et al. 2008). Typically, they employ sideways and diagonal walking with an alternating tetrapod gait (Vidal-Gadea et al. 2008) that may aid in tracking threats visually (Domenici et  al. 2011b), although some (e.g., soldier crabs, Mictyris longicarpus, and Libinia emarginata) employ forward- and backward-walking patterns that are similar to the macrurans or macruran-like lobsters (Nalbach 1990). Due to differences in thorax width-to-length ratios and leg joint angles, crabs that employ sideways walking have an increased walking speed compared to those employing forward walking. Vidal-Gadea et al. (2008) argue that, as a result, one should see lighter weight carapaces on sideways-moving crabs (e.g., Carcinus, Cancer, Callinectes spp.) and thicker carapaces on forward-walking crabs (e.g., Libinia and other majids). Such differences in thickness may also lead to differences in decorating behaviors and spinous extensions of carapace margins. When approached or attacked, a crab attempting to escape must run, walk, or swim faster than the predator, but no studies have examined if crabs can outpace their predators, and few studies have provided information on walking speeds. Speeds seem to vary from less than 0.01 m/s−1 (red king crabs; Jørgensen et al. 2007) to 35 m/s–1 (N. granulata; Oliva et al. 2007). Although they lack a large, powerful abdomen, a number of brachyuran crabs are capable of swimming, but they use a mechanism different from that of shrimp or lobsters (Hartnoll 1971, Boudrias 2013). Crabs in the family Portunidae have the best developed swimming abilities due to modifications of their legs, carapace, and musculature. The fifth pereopods end in oar-like paddles that act as hydrofoils (providing both lift and thrust) and, due to alteration in the coxal-sternal articulation, these legs can rotate 90 degrees relative to the body (Hartnoll 1971). Their carapace shape (more elongated than rounded) results in less drag (because of sideways swimming) and helps to generates sufficient lift to overcome weight above buoyancy (Hartnoll 1971, Blake 1985). They can both hover and swim sideways, achieving burst speeds up to 0.5 m/s−1 and can maintain swimming speeds of 0.1–0.2 m/s−1 (Blake 1985, Carr et al. 2004, Zimmer-Faust et al. 1994). Galatheid crabs represent a group that is intermediate between macrurans and/or macruran-like reptantians and the reptantian crabs. They can swim backward by extending and flexing their abdomen in a manner that is homologous to shrimp and lobsters (Sillar and Heilter 1985, Wilson and Paul 1987). When disturbed, the crab extends its tucked abdomen 53–80 degrees (usually larger extensions are seen in the first two tail flips) and generally flares its tailfan and then flexes—this differs from the macruran response of first flexing an already extended abdomen and then extending it again for the next cycle of flexion. They can maintain tail flips up to 50 cycles of extension and flexion. Again, as with all other decapods studied, it is unknown how effective such actions are against attacking predators. Clinging Some species of decapods are capable of using their pereopods to hold onto complex substrates with great force, thereby resisting attempts by the predator to flip them over (where the less calcified ventral surface would be accessible). Barshaw and Spanier (1994) showed that Mediterranean slipper lobsters used their short, strong legs to grasp the substrate and resist being dislodged. Spanier and Lavalli (1998) reported that the force needed to dislodge Mediterranean slipper lobster clinging to a rough substrate (outside of the water) can reach maximum magnitudes of 3–15  kg (~8–29 times the body weight of the lobster) and linearly correlates with lobster size. Briones-Fourzán et  al. (2006) compared clinging in two sympatric species of spiny lobsters, Panulirus argus and P.  guttatus, and found that clinging strength was directly related to size (as measured by carapace length). In crabs (Grapsus tenuicrustatus), mean maximum clinging force on rugose or volcanic rock ranged from 4.9 to 20.7 N (more than an order of magnitude times the body weight; Martinez 2001). Unfortunately, this phenomenon has not been well studied in a

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Predator Adaptations of Decapods variety of decapods. It seems logical to assume that crabs, shrimp, and other decapods that cling to rocky surfaces, corals, algae, and seaweed blades may exert grasping force as one of their antipredatory strategies, but such assumptions will require rigorous testing to show the efficacy of such behavior and its frequency of use. Warning Colorations A few decapods bear marking patterns that are highly conspicuous for the habitats in which they dwell. Some xanthid crabs, notably Lophozozymus species that contain a paralytic palytoxin in their flesh, have a red/orange and white coloration pattern that may serve as a warning signal, similar to that seen in poisonous snakes or butterflies (Ng and Chia 1997). Because these crabs live along shores and in coral reefs, their coloration pattern should be fairly conspicuous. Other toxic xanthids, Zosimus aeneus and Demania alkali, are less conspicuous, having coloration patterns of purple-mauve-orange or green with white and brown markings; these crabs also contain a saxitoxin analog and tetrodotoxin (Yasumoto et al. 1986). Iridescent colors are known in several crustaceans and could also play a role in escaping or avoiding predation, especially if those colors are used as a warning signal to deter attacks or approaches (Doucet and Meadows 2009). Inbar and Lev-Yadun (2005) argue that conspicuous and colorful spines in crustaceans, such as the blue-red-white spines on the legs of the swimming crab, C. sapidus, may also serve as visual aposematic signals. Staaterman et al. (2010) made a similar suggestion for the spines of the California spiny lobster, Palinurus interruptus, and Bouwma (personal communication) has suggested that the spotting pattern seen on the anterior surface of the cephalic region of spiny lobsters also may be a warning signal. Clearly, this is an area of research that needs to be pursued. Aposematic Sounds In a world where light penetrates only so far and where certain wavelengths of light are rapidly lost, aposematic coloration patterns may only be useful in shallow and clear waters. Hence, we see the use of sound by many different decapods that possess a mechanism for sound production (Moulton 1957, 1958, Popper et al. 2001). Currently, most of the studies on sound have focused on how species can use sounds to stun their prey, but recent studies have begun to focus on how sound can be used to repel predators during a predatory interaction (Bouwma and Herrnkind 2009, Buscaino et al. 2011, Ward et al. 2011). Snapping shrimp produce sounds by rapidly closing one of their front chelae, snapping the ends together to generate a loud click (Au and Bank 1998). Versluis et al. (2000) suggest that snapping in Alpheus spp. serves multiple roles: at short distances (~3 mm), the snapping can kill or stun small prey whereas at a greater distance, it can be used for intraspecific interactions (Wicksten 2010) and perhaps also to deter approaching predators. Some spiny lobsters (the “Stridentes”) are known to produce sounds when interacting with potential predators. These acoustic signals are broad-frequency bandwidth sounds (“rasps”) that are produced by a “stick and slip” frictional movement that occurs when macroscopically smooth files with microscopic shingles at the base of the antenna are drawn over the soft tissue ridges of the plectrum that run in an anteroposterior direction (Moulton 1957, Patek 2001, Patek and Baio 2007). Bouwma (2006) demonstrated that the spiny lobsters Palinurus argus and P. guttatus produced sounds during encounters with the predatory triggerfish Balistes capriscus that were effective in decreasing future encounters when combined with a whipping motion of the long, spinous antennae. Bouwma and Herrnkind (2009) further demonstrated that if spiny lobsters produced sounds when they were attacked and grasped by Octopus briareus, they were more likely to escape unharmed. Buscaino et al. (2011) reported that significantly more sounds were emitted by solitary



Kari L. Lavalli and Ehud Spanier

spiny lobsters (Palinurus elephas) during predatory encounters than by grouped lobsters, and sounds always accompanied lunging and whipping behavior of the antennae. Hence, it is likely that sound production capabilities evolved in spiny lobsters at least in part to help deter predators. Although the stridente clade of spiny lobsters has an actual apparatus for creating sound, other species of lobster may be able to use contracting muscles to generate vibrational sounds. Ward et al. (2011) investigated the influence of two potential fish predators of American lobsters, Homarus americanus  —cod (Gadus morhua) and striped bass (Morone saxatilis)—on the production of sounds by vibration of their dorsal carapace (Henninger and Watson 2005). Although solitary lobsters spontaneously produced sounds at a low rate (1.2 ± 0.23 sound events per 30 min), the presence of a single fish predator led to an increase in the rate of sound production (cod: 51.1 ± 13.1 events per 30 min; striped bass: 17.0 ± 7.0 events per 30 min). Direct contact with the predator was not required to generate sound because most of the sound occurred when a fish came within 0.5 m of a lobster. Fish turned and swam away significantly faster when lobsters produced sound than when lobsters were silent. Additionally, after striped bass (but not cod) experienced a number of these sound events, they subsequently avoided swimming close to the lobsters. Thus, Ward et al. (2011) suggest that sound production by American lobsters may serve to deter potential fish predators. Clearly, this is an area where more work on a variety of taxa needs to be done. Responses to Predatory Attack and Attempts at Subjugation Armor Benthic decapod exoskeletons come in a variety of shapes and thicknesses and are often modified by spines and other constructional aspects that add strength or act to blunt cracks. Furthermore, the decapod exoskeleton is layered in such a way to also add strength (Dillaman et al. 2013), and additional layers are added with growth to larger body sizes, something that is not seen in pelagic species (Pütz and Buchholz 1991, Amato et al. 2008). Because shell strength and resistance to breakage increase as the third power of shell thickness (Wainwright et al. 1976), slight increases in thickness should result in substantial increases in force needed to fracture the shell. Hence, decapods can add small amounts of additional layering to gain more strength and only minimally affect their density to still allow for effective escape behaviors. Whatever increases in density that occur with greater skeletal thickness also allow for greater stability on the benthic environment if living in wave- or current-swept environments (Amato et al. 2008). For some species, attainment of large size essentially provides a refuge from most predators because few predators can successfully handle their thicker shells (Werner and Gilliam 1984, Wahle and Steneck 1992). Body size can also influence the antipredatory strategy to be used by decapods (e.g., “fight or flight”; Wasson and Lyon 2005), with larger animals being more likely to stand their ground and fight than smaller animals. The shell covering is usually thicker and more calcified in the more exposed parts of the body of many decapods (e.g., dorsolateral carapace and appendages such as legs, claws, and antennae), although all studies thus far indicate that the dorsal carapace is thinner and less hardened than the exoskeleton of the chelae (Waugh et al. 2006; Fig. 8.7A–D). Few studies have actually examined the force needed to fracture or break the cuticle of the carapace or the claws. Those forces needed for breakage of carapace cuticle can range from 3 to 25 kg in lobsters (Barshaw et al. 2003) and crabs (MacDonald et al. 2007) to 30 MN m−2 for C. maenas (Wainwright et al. 1976). In the crabs studied, carapace width rather than shell thickness is a better predictor of force needed to damage the cuticle (MacDonald et al. 2007), and areas with denticles/tubercles are significantly harder than smooth regions (Waugh et al. 2006).

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Fig. 8.7. Armor in decapods, photos by authors from Smithsonian Museum collections. Thick armor of crabs: (A) Calappa flamma, (B) Pilumnus sp., (C) Menippe mercenaria, (D) Dromidia antillensis. Protective spines: (E) seen over the eyes of spiny lobsters, Palinurus elephas. Spines used to increase size of crabs or to make them unpalatable: (F) Neolithodes grimaldi, (G) Homolochunia valdiviae, (H) Anamathia rissoana, (I) Acanthocarpus bispinosus, ( J) Hypothalassia armata, (K) Callinectes danae.



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In addition to the armor provided by a mineralized, layered exoskeleton (Fig. 8.7A–D), many species modify their shell with spines (Fig. 8.7E–K). Spines on appendages and the carapace surface may act to make it difficult for a predator to reach or penetrate the exoskeleton (Fig. 8.7F,G,H); may protect vulnerable body parts, such as eyes (e.g., orbital spines; Fig. 8.7E); or may keep the attacker at a distance (e.g., the long, spinous antennae; Fig. 8.7E). Spines may also be used to increase the overall size of the animal (e.g., long, lateral spines seen on many crabs, long dorsal spines on some crabs) to possibly exceed gape width of the predator or to make the prey painful to swallow (e.g., numerous spines along the carapace margins in many crabs; Fig. 8.7H,J,K). Many subtropical and tropical species bear spines all over their dorsal carapace, and some of the macruran-like forms may also have spines on the lateral edges of the pleonal segments. Temperate and Arctic forms, while bearing some spines, do not show the same density across their entire dorsal surface. Based on many studies showing that predation pressures are greater in more tropical latitudes (Vermeij 1987), it may follow that decapods at lower latitudes were subject to greater predation pressure by shell-breaking predators, and such pressure provided the selective impetus for the evolution of additional cuticular structures that would strengthen shells. Along these lines, shell-breaking predators have been cited as the evolutionary driving force behind the increase in shell strength among gastropods living at lower latitudes (Vermeij 1987). However, there are alternative hypotheses for the evolution of spines: they may arise to reduce settlement of epibionts, may serve as camouflage by breaking up the outline of the shell, or may simply be a remnant of larval life, where they may serve as keels for a pelagic existence (Walker and Brett 2002). Additionally, the lower latitudes (tropics in particular) have calcium carbonate that is supersaturated in seawater, and this may have made it less energetically costly to make spines (Walker and Brett 2002). In regions where shell-breaking predators are common, alternatives to spines would be to form raised tubercles that would confer more strength or to extend the carapace edges over the legs so that the legs could be protected. This latter strategy is used in the calappids, and both are used in the scyllarids (Fig. 8.7A). Weapons Weapons come in many forms in decapods: they can be claws, sharp dactyls on pereopods, or sharp whipping antennae, and they can also be other animals that are carried and used aggressively (i.e., anemone-carrying crabs). Weapons may keep the attacker at bay, but might make the animal more noticeable (Dingle 1983). They may also reduce the efficacy of flight responses due to their mass and inertia, and they may interfere with the hydrodynamics of escape swimming by increasing drag. In contrast, having both strong armor and weapons might reduce the need to flee ( Janzen 1981, Ydenberg and Dill 1986), whereas combined weaponry of grouped animals likely improves the ability to fend off an attacker (Zimmer-Faust and Spanier 1987, Lavalli and Herrnkind 2009). The most diverse and extreme crustacean weapons are the enlarged, often highly sexually dimorphic chelipeds of many decapods (shrimp, crayfish, nephropid lobsters, and crabs; Emlen 2008) that can injure or even deliver fatal blows to predators (Fig. 8.8A–D). Chelipeds can be used to pinch the predator or shield the decapod from attack (as per Wasson and Lyon 2005). However, chelipeds are used by males as weapons or displays in contests over females, food, or burrows (Emlen 2008) and for gathering/capturing and crushing food, and they may function in constructing shelters and burrows for defense or reproduction (Lee 1995, Mariappan et al. 2000). As a result, their design may not be optimal for any one particular purpose. The long spinous antennae of palinurids presumably are used for probing spaces or conspecifics and as weapons. The antennae are often as long as, if not longer than, the entire body of the lobster (Fig. 8.8E,F) and are constructed so that the spines along their surface face outward, much

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Fig. 8.8. Examples of enlarged chelae that lobsters, shrimp, and crabs can use as weapons. Photos by authors from Smithsonian Museum and Stazione Zoologica Napoli Museum collections. (A)  Asymmetric chelae of Carpilius maculates, (B) symmetric claws of Pseudozius (Euryozius) bouvieri, (C) large clawed lobster, Homarus americanus, (D) the slender, elongated claws of Nephrops norvegicus, (E) and (F) the long spinous antennae and spinous carapace of the spiny lobster, Palinurus elephas.

as thorns do on plants. The animals can sweep these antennae forward, sideways, and backward and can therefore protect their entire dorsal surface. When under attack by piscine predators, they typically point the antennae toward the fish, essentially keeping it at a one-antenna distance. If the fish should come in closer to the body, the antennae can be brought forward and medially to whip at and smack the fish with its spines (Lavalli and Herrnkind 2009, Buscaino et al. 2011). This generally drives the fish backward. Barshaw et al. (2003) found that weapons come with two major costs: the need for vision to properly aim them at an approaching predator and the need for the joints controlling the movement of the weapons to remain intact and functional. Such weapons are rendered ineffective if predators are able to bite off eyestalks or damage the merus-carpal joint of the claw or the basal segments of the antennae. Antennae can also be slowly bitten down to a length at which they are ineffective at keeping the predator away from the rest of the body (Parsons 2003, Lavalli, personal observations). Loss of a single weapon of a pair (via autotomy or severe damage) may result in the prey individual having to increase its activity to fend off predators but may not necessarily increase the likelihood of attack or death (Barshaw et al. 2003, Parsons 2003; Fig. 8.9A,B). However, if the weapon is associated with aposematic signaling (via sound-generating organs), inability to signal may make the weapon less effective (Bouwma 2006; Fig. 8.9C). What seems most important in determining the effectiveness of a weapon is the actions of the individual. Hence, for animals willing to exert energy to essentially “parry” via various actions (weapon pointing, swiveling around as the predator moves, etc.) and attack (whipping, displaying, punching, lunging, etc.) approaching predators, the likelihood of successful attack diminishes (Parsons 2003, Lavalli and Herrnkind 2009). Unfortunately, all weaponry is assumed to be beneficial to the individual possessing it, and this assumption has

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Fig. 8.10. Anemone weapons that are carried by the pom-pom crab, Lybia edmondsoni, drawn by Tamara Clark.

only been rigorously tested in lobsters (Barshaw et al. 2003, Parsons 2003, Bouwma 2006, Lavalli and Herrnkind 2009, Bouwma and Herrnkind 2009, Buscaino et al. 2011). Similar studies need to be conducted for crabs with well-developed claws. Some brachyurans are unusual in that they have been observed to use other animals as weaponry (Fig. 8.10). Xanthid crabs (Lybia spp. and Polydectus spp.) carry minute anemones in each chela by means of a small hook that embeds in the anemone column (Duerden 1905). Lybia spp., known as “boxer crabs,” position their claws with the anemones attached in front of their body and advance with one claw held forward and then the other, similar to the way a boxer moves (Guinot et al. 1995). Homolid, dorippid, and some dromiid crabs hold anemones, gorgonians, colonies of soft corals, or sponges in the chela or subchelae of their fifth pereopods (Guinot et al. 1995). These pereopods are modified so that they can move dorsally and up above the carapace, perpendicular to the crab’s body. It is assumed that these associations with stinging organisms would provide protection from predators and/or aggressive interactions with other conspecifics; however, only one study has been performed testing the latter hypothesis, and, in this case, the crabs never used the anemones against one another and, in fact, held the anemones to the side so that they would not be damaged during wrestling episodes (Karplus et al. 1998). Limb Autotomy and Autospasy Autotomy (the voluntary shedding of limbs or other body parts in the face of predation via a breakage plane by means of a reflex) and autospasy (the severance of an appendage at a preformed fracture plane when the appendage is pulled by the predator against resistance by the prey) are highly effective escape mechanisms that have evolved independently in a variety of taxa of decapods (e.g.,



Kari L. Lavalli and Ehud Spanier

cancrid, grapsid, majoid, menippid, portunid, pilumnid, pseudothelphusid, ocypodid, raninid, xanthid crabs, and porcelain crabs, as well as in squat lobsters, spiny lobsters, alpheid, mud shrimp, and palaemonids; see Fleming et al. 2007 for an extensive review). Costs associated with loss of an appendage depend largely on which appendage was shed and how long it takes to regenerate the appendage. For example, decapods that lose a cheliped that was used to crush food or graze algae may have to shift their diet if another leg cannot assume the lost appendage’s function and regeneration takes a number of molts to achieve (Smith 1990, Juanes and Smith 1995). If the cheliped was also used in intraspecific displays and/or defense, then autotomized individuals may become subordinates, securing fewer matings (Smith 1992, Juanes and Smith 1995) or facing more frequent eviction from shelters (Berzins and Caldwell 1983, O’Neill and Cobb 1979). Similarly, loss of legs may affect gait speed, which can impact the movements the animal undertakes to find mates, food, and shelter within its home range or the speed at which an individual can move during migrations (Fleming et  al. 2007). Loss of antennae can have dramatic impacts, especially if such antennae are used in food capture (e.g., porcelain crabs) or in defense (e.g., spiny lobster; Barshaw et al. 2003). When appendages that can be used as weapons are lost, survival can be dramatically impacted: several species of crabs (Dungeness, spanner, and stone crabs) suffer increased mortality with the loss of one or more appendages (Fleming et al. 2007), and spiny lobsters suffer nearly 100% mortality with the loss of both spinous antennae (Barshaw et al. 2003, Parsons 2003; but see laboratory studies on green shore crabs with multiple limbs autotomized and spiny lobster with a single antennae autotomized that show no increased mortality: Kuris and Mager 1975, Parsons 2003). Growth rates might also be depressed; however, Frisch and Hobbs (2011) studied the effects of autotomy on long-term survival and growth rates of tagged painted spiny lobsters and found that recapture and mean annualized growth rates of uninjured, minimally injured, and moderately injured lobsters were not significantly different. They suggest that the energetic cost of a single episode of autotomy is either negligible or exists as a trade-off with some other life history trait, such as reduced reproductive performance. After losing an appendage, decapods may shift individual strategies toward predator avoidance, such that the animal becomes more risk averse because defensive or offensive strategies may be limited; this increase in risk aversiveness may depress somatic growth rates that would allow for more rapid regeneration of the lost appendage (see Juanes and Smith 1995 and Fleming et al. 2007 for a review; see Frisch and Hobbs 2011 for an alternate view). Given these costs, autotomy of appendages is not a response that is readily given in most species and may become even less likely after autotomy of one limb has already occurred (but see porcelain crabs that have hair-trigger autotomy of limbs; Wasson et al. 2002). Essentially, autotomy of an appendage requires a complex decision-making process between two mutually exclusive strategies: immediate flight or fight with potentially delayed flight. Wasson and Lyon (2005) argue that—at least for porcelain crabs (Petrolisthes spp.)—a number of factors affect an individual’s decision to autotomize an appendage, and those decisions may be context-dependent based on an analysis of the costs and benefits of limb loss. So, for example, smaller crabs and females (generally smaller than males) were more likely than larger crabs to escape by autotomizing rather than by struggling and pinching. In the cases of both size and sex, larger chelae came with larger body size and likely conferred greater benefits in terms of fighting strength and territorial defense, making retention more important (Wasson and Lyon 2005). It is probable that most decapods demonstrate this kind of adaptive flexibility, employing the costly strategy of autotomizing a limb as a last resort only when their chance at success by struggling is low. Group Aggregation and Defense Various models have been proposed to explain the potential antipredatory benefits of group formation. Individuals in groups may have a lower per capita risk of predation by dilution or by a selfish herd response, by increased predator detection/vigilance, or by cooperative defense once

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Predator Adaptations of Decapods attacked (Hamilton 1971). It seems likely that individuals in groups potentially benefit from more than one of these mechanisms, although few studies have experimentally examined such multiple benefits (Dehn 1990). Observations of various decapod species in the field reveal potential defensive formations, such as the rosette (or phalanx) formations seen in spiny lobsters (Herrnkind et  al. 2001)  and the pods seen in slipper lobsters (Lavalli and Spanier 2001)  and majid crabs (DeGrousey and Steward 1985, Stevens et al. 1992, 1994, Sampedro and González-Gurriarán 2004; Fig. 8.11A,B). Some argue that the gregarious habit is not new for decapods and may have been displayed by the eryonids as far back as the Jurassic when small groups would take up residence in ammonoid shells at the bottom of the sea to avoid fish predators (Klompmaker and Fraaije 2012) or from the Cretaceous when primitive palinurid lobsters would share burrows (Bromley and Asgaard 1972, Tsujita 2003). For spiny lobsters in the field, grouping together initially provides hydrodynamic benefits in drag reduction when traveling on featureless terrain (Bill and Herrnkind 1976), but it also allows formation of pods (“rosettes”) when a predator approaches the migrating lobsters. Grouping in pods provides significantly higher survivorship against piscine predators than predicted by dilution models only, and individual lobsters within the group structure expend less energy per capita than do solitary lobsters in fending off attacks (Lavalli and Herrnkind 2009; Fig. 8.11C), even though numbers of behaviors may be high overall during encounters (Buscaino et al. 2011). In most cases, many of the offensive behaviors (pointing, parrying, whipping and/or lunging with spinous antennae at the predator) are accompanied by sound emissions (Buscaino et al. 2011). Gregarious behavior seems to be context-sensitive, and those species displaying it can alter their responses when faced with different kinds of predators or differing predation risks (Briones-Fourzán and Lozano-Álvarez 2008). Generally, solitary reef-dwelling lobsters (Palinurus guttatus) that are subject mostly to sit-and-wait predators do not aggregate when predator density increases, but do aggregate with increasing density of conspecifics, suggestive of a guide effect to appropriate shelters within reef complexes. However, when faced with highly mobile, searching predators, these lobsters will form pods that may confer dilution effect advantages to individuals within the pod (Briones-Fourzán and Lozano-Álvarez 2008). Nevertheless, when octopuses or blue crabs are presented as predators, both social and solitary spiny lobsters abandon groups and adopt individual strategies that differ significantly in both offensive and defensive behaviors used (Bouwma, personal communication, Buscaino et al. 2011). This suggests that a gregarious habit in many spiny lobster species and cooperative defense in some spiny lobsters may have evolved specifically for fending off piscine predators rather than predators in general. Slipper lobsters also group together, but they do not co-defend because they lack any weapons with which to do so. Instead, clumping together seems to confuse the predator and delay an attack (Lavalli and Spanier 2001), which, in the short term, would benefit individuals in the group and buy time to move away from the predator even as individuals, since multiple escaping individuals would further confuse a predator’s sensory system and make it hard to target a specific one to chase. Likewise, majid crabs are known to form pods ranging in size from 5 to more than 1,000 individuals (Fig. 8.11B), but they do so only in very specific seasons (mating and molting) and in relatively shallow waters (2–10 m is most common, but pods have also been seen at 150 m; Sampedro and González-Gurriarán 2004). In analyzing the actual structure of the pod, Sampedro and González-Gurriarán (2004) found that pods were pyramidal in shape, with intermolt animals on the outer surface and soft postmolt animals more centrally and interiorly located. They suggest that this arrangement provides protection to the most vulnerable members of the group by placing the harder shelled individuals in a position where they might be able to better withstand attacks. Sampedro and González-Gurriarán (2004) argued that it was unlikely that the pods were used to facilitate mating given that spider crabs appear to mate during intermolt rather than at the molt. A number of authors (Baal 1953, Le Sueur 1954, Števčić 1971) also noted that when octopuses are

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Predator Adaptations of Decapods present in the area, spider crabs in the intermolt stage form pods, suggesting that they are employing some kind of dilution or selfish herd strategy to decrease individual predation rates. In portunids, pod formation seems to occur to synchronize molting among individuals within a specific area, such that newly molted individuals would be less subject to cannibalistic attacks by conspecifics (Hines et al. 1987, Ryer et al. 1990). Responses to Consumption by Predator Use of Noxious Chemicals Although crustaceans use chemical cues for many behaviors, including to assess threats such as the presence of predators (Hay 2011), and more than half of all terrestrial arthropod orders contain species using chemical deterrents, such deterrents are not known in the Decapoda (Whitman et al. 1990) and, unlike terrestrial arthropods, where many species are venomous, only a few crustaceans have been identified as having poisons present in their flesh. However, Wicksten (2010) reports that the deep-water caridean shrimp Systellapsis debilis can expel luminous secretions. These secretions can potentially confuse or repel potential predators. Additionally, some decapods can make use of the noxious chemical weaponry/secretions of their symbiont associate (e.g., cnidarians, various species of attached algae; Guinot et al. 1995, Stachowicz and Hay 1999, Hultgren and Stachowicz 2009) to repel predators and avoid being consumed. Alarm Cues As in other marine animals (Chivers and Smith 1998, Hazlett 2011), it would seem advantageous for decapods to use cues that would help them assess predation risk. These cues could be chemical in nature such that the prey “smells” the predator or the predator’s consumption activities if downstream or could be hydrodynamic in nature such that the prey “feels” the predator when water disturbances are transmitted to sensory hairs on its exoskeletal surface. Numerous studies have examined the sensory capabilities of decapods in detecting both odors and water displacement (Breithaupt and Thiel 2011). Fewer have combined predator odors with behavioral responses of the potential prey, but, in those studies, it is clear that decapods can detect both piscine and cephalopod odors and actively avoid areas with predators (Berger and Butler 2001) or alter behavior in a manner to reduce predator risk (Hazlett 2000, Sakamoto et al. 2006). Additional cues can come from injured or killed conspecifics or heterospecifics via release of hemolymph into the surrounding water or via urine release. “Alarm odor” released by hemolymph emitted by injured individuals is known for some species of lobsters (Briones-Fourzán 2009, Lavalli, personal observation). All of these chemicals may initiate appropriate behavioral responses in the alerted animals including avoidance of their source areas, immobility (freezing), watchful postures, reduction of activity, or increased use of shelters and refuges. For example, when gregarious spiny lobsters are given a choice between shelters with intact conspecifics, shelters with autotomized conspecifics, and shelters with injured and bleeding conspecifics, they choose intact individuals, avoid injured individuals, and show a random response to autotomized individuals (Parsons and Eggleston 2005, Briones-Fourzán 2009). Likewise, blue crabs avoid food-baited traps that contained injured conspecifics (Ferner et al. 2005). The brachyuran Heterozius rotundifrons increases the duration of a defensive posture it adopts when exposed to crushed conspecifics (Hazlett and McLay 2000) and crushed heterospecifics (especially other brachyurans; Hazlett and McLay



Kari L. Lavalli and Ehud Spanier

2005), whereas snapping shrimp increase their frequency of displaying in the presence of crushed conspecifics (Hazlett and Winn 1962). Except for spiny lobster (Shabani et  al. 2008), the sensory organs detecting such cues have not been identified. Furthermore, most of the studies conducted have been in laboratory settings, so it is not clear how odor plumes from injured or damaged conspecifics would be detected in the field and how contingent prey behavior would be on other factors such as hunger level (possibly decreasing risk aversive behavior), proximity to shelter, and prior experience with the predator, as well as efficacy of other avoidance or antipredator responses. Poisons, Lethality The occurrence of poisonous crabs has been known for centuries: Rumphius (1705) wrote about a crab from Ambon that he had named “Cancer saxatilis,” stating that it was very poisonous (Ng and Chia 1997). Some Asian and Australian species of xanthid crabs, as well as some Asian reef crabs, are known to contain paralytic toxins in their flesh. These include Lophozozymus pictor (probably Cancer saxatilis) and Lophozozymus erinnyes that contain a paralytic palytoxin (Ng and Chia 1997), and Z. aeneus and D. alkali, which contain a saxitoxin analog and tetrodotoxin (Yasumoto et al. 1986). In L. pictor, the highest concentrations of toxin is found in the gut and hepatopancreas, whereas muscle is less toxic and the carapace is only mildly toxic; however, this toxicity can dissipate over 24 days until all tissue is cleared of it, which suggests that the source of toxin is from food (Chia et al. 1993). Kotaki et al. (1983) determined that the source of toxicity in reef crabs Z. aeneus and Atergatis floridus was from their food—either a calcareous red alga (Jania sp.) or bivalves that had fed on toxic marine algae. Consumption of these species can cause death, and predators would learn to avoid them much in the same way that bird predators learn to avoid monarch butterflies. Thus far, however, no experiments examining predator responses to these crabs have been conducted, and current studies have only focused on the effects these crabs have on humans consuming them.

FUTURE DIRECTIONS Most of the studies in the past four decades have focused on decapod predator avoidance mechanisms such that we have a fairly good understanding of these strategies for a large variety of species in all decapod families. Fewer studies have focused on antipredator mechanisms and, where such studies have been conducted, they have focused on only one or several families. As a result, we still know little about how effective those antipredator strategies are during predatory encounters. Decapods provide a remarkable model by which to test multiple hypotheses concerning the costs and benefits of individual strategies, as well as the behavioral plasticity that might be shown when competing interests (such as feeding, mating, or molting) arise. The differences in species-tospecies shell architecture and internal design allow for hypothesis testing for questions concerning the function of tubercles, spines, thickness changes, alterations in escape response, and decoration patterns. The fact that so many different kinds of predators prey on decapods allows one to examine which strategies are successful against different predator types (gulpers/swallowers, biters, smashers, etc.). Behavioral plasticity within species allows for the determination of which strategies appear under which contexts and why. This chapter has sought to provide a framework through which future investigators can determine what work remains to be done to better understand how benthic decapods, many of which are commercially important to humans, reduce the

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CONCLUSIONS Mobile, benthic decapods are a highly diverse and have colonized all areas of the oceans, as well as intertidal and sandy beach zones. The modern forms have ancient roots that go back to the Triassic and Jurassic and subsequently expanded and radiated into numerous forms in the Cretaceous. They have had to contend with cephalopods, other crustaceans, marine reptiles, ancient and modern sharks, ancient and modern teleosts, marine birds, and marine mammals. As a result of their widespread distribution and the variety of predators to which they have been exposed over millions of years, they have evolved a wide variety of predator avoidance and antipredator mechanisms for survival. These diverse mechanisms, along with the behavioral plasticity to change from one strategy to another, have allowed the decapods to inhabit all oceans and nearly all types of substrates, becoming one of the most successful taxa in the marine realm.

ACKNOWLEDGMENTS We are extremely grateful to the staff of the Invertebrate Collections at the National Museum of Natural History, Smithsonian Institution, for permitting us access to their decapod collection for photographs. We are also grateful for the various people who graciously offered up photographs of decapods for use in the figures: Michael Childress, Staff of the Massachusetts Department of Marine Fisheries, Guido and Phillippe Poppe, and John Stachowicz.

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Tsujita, C.J. 2003. Smothered scampi: taphonomy of lobsters in the Upper Cretaceous Bearpaw Formation, Southern Alberta. Journal of Taphonomy 1:185–204. Vermeij, G.J. 1987. Evolution and escalation. Princeton University Press, Princeton, NJ. Versluis, M., B. Schmitz, A. von der Heydt, and D. Lohse. 2000. How snapping shrimp snap: through cavitating bubbles. Science 289:2114–2117. Vidal-Gadea, A.G., M.D. Rinehart, and J.H. Belanger. 2008. Skeletal adaptations for forwards and sideways walking in three species of decapod crustaceans. Arthropod Structure and Development 37:56–108. Wahle, R.A. 1992. Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65:52–60. Wahle, R.A., and R.S. Steneck. 1992. Habitat restrictions in early benthic life: experiments on substratum selection and in situ predation with the American lobster. Journal of Experimental Marine Biology and Ecology 157:91–114. Wainwright, S.A., W.D. Biggs, J.D. Currey, and J.M. Gosline. 1976. Mechanical design in organisms. Edward Arnold, London, U.K. Walker, S.E., and C.E. Brett. 2002. Post-Paleozoic patterns in marine predation: was there a Mesozoic and Cenozoic marine predatory revolution? Pages 119–193 in M. Kowalewski and P.H. Kelley, editors. The fossil record of predation, Vol. 8, The Paleontological Society Papers, Paleontological Society, New Haven. Ward, D., F. Morison, E. Morrissey, K. Jenks, and W.H. Watson, III. 2011. Evidence that potential fish predators elicit the production of carapace vibrations by the American lobster. Journal of Experimental Biology 214:2641–2648. Warman, C.G. 1990. Rhythmic behaviour of coastal crustaceans. Ph.D. thesis, University College of North Wales, Bangor, U.K. Wasson, K., and B.E. Lyon. 2005. Flight or fight: flexible antipredatory strategies in porcelain crabs. Behavioral Ecology 16:1037–1041. Wasson K., B.E. Lyon, and M. Knope. 2002. Hair-trigger autotomy in porcelain crabs is a highly effective escape strategy. Behaviour Ecology 13:481–486. Waugh, D.A., R.M. Feldmann, A.M. Schroeder, and M.H.E. Mutel. 2006. Differential cuticle architecture and its preservation in fossil and extant Callinectes and Scylla claws. Journal of Crustacean Biology 26:271–282. Weihs, D., and P.W. Webb. 1984. Optimal avoidance and evasion tactics in predator-prey interactions. Journal of Theoretical Biology 106:189–206. Weiss, H.M., E. Lozano-Álvarez, and P. Briones-Fourzán. 2008. Circadian shelter occupancy patterns and predator-prey interactions of juvenile Caribbean spiny lobsters in a reef lagoon. Marine Biology 153:953–963. Werner, E.E., and J.F. Gilliam. 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15:393–425. Whitman, D.W., M.S. Blum, and D.W. Alsop. 1990. Allomones: chemicals for defense. Pages 289–351 in D.L. Evans and J.O. Schmidt, editors. Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, NY. Wicksten, M.K. 1979. Decorating behavior in Loxorhynchus crispatus Stimpson and Loxorhynchus grandis Stimpson (Brachyura, Majidae). Crustaceana (Supplement) 5:37–46. Wicksten, M.K. 1993. A review and model of decorating behavior in spider crabs (Decapoda, Brachyura, Majidae). Crustaceana 64:314–325. Wicksten, M.K. 2010. Infraorder Caridea Dana, 1852. Pages 165–206 in J. Forest and J.C. von Vaupel Klein, editors. The Crustacea, Traite de Zoologie 9A—Decapoda. Koninklijke Brill, Leiden/Boston. Wieters, E.A., S.M. Januario, and S.A. Navarrete. 2009. Refuge utilization and preferences between competing intertidal crab species. Journal of Experimental Marine Biology and Ecology 374:37–44. Wilson, K.A., K.W. Able, and K.L. Heck. 1990. Predation rates on juvenile blue crabs in estuarine nursery habitats: evidence for the importance of macroalgae (Ulva lactuca). Marine Ecology Progress Series 58:243–251. Wilson, L.J., and D.H. Paul. 1987. Tailflipping of Munida quadrispina (Galatheidae): conservation of behavior and underlying musculature with loss of anterior contralateral flexor motoneurons and motor giant. Journal of Comparative Physiology 161A:881–890.

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Predator Adaptations of Decapods Wine, J.J., and F.B. Krasne. 1972. The organization of escape behaviour in the crayfish. Journal of Experimental Biology 56:1–18. Yamashiro, H. 1999. Masking behaviour in a commensal shrimp, Metapontonia fungiacola Bruce, 1967 that uses the soft tissues of the host coral (Decapoda, Palaemonidae, Pontoniinae). Crustaceana 72:307–312. Yasumoto, T., D. Yasumura, Y. Ohizumi, M. Takahashi, A.C. Alcala, and L.C. Alcala. 1986. Palytoxins in two species of xanthid crabs from the Philippines. Agricultural and Biological Chemistry 50:163–167. Ydenberg, R.C., and L.M. Dill. 1986. The economics of fleeing from predators. Advances in the Study of Behavior 16:229–246. Yu, X., X. Zhang, P. Zhang, and C. Yu. 2009. Critical swimming speed, tail-flip speed and physiological response to exercise fatigue in kuruma shrimp, Marsupenaeus japonicus. Comparative Biochemistry and Physiology A153:120–124. Zimmer-Faust, R.K., and E. Spanier. 1987. Gregariousness and sociality in spiny lobsters: implications for den habitations. Journal of Experimental Marine Biology and Ecology 105:57–71. Zimmer-Faust, R.K., D.R. Fielder, K.L. Heck, L.D. Coen, and S.G. Morgan. 1994. Effects of tethering on predatory escape by juvenile blue crabs. Marine Ecology Progress Series 111:299–303.

9 SMALL FREE-LIVING CRUSTACEANS

Richard B. Taylor

Abstract Small free-living crustaceans (SCs) are abundant in many benthic habitats, where they play important ecological roles as consumers and as prey for higher trophic levels. SC lifestyles are heavily influenced by requirements for suitable food and shelter from predators and environmental stresses. Their desirability as prey and their general lack of intrinsic structural or chemical defenses typically mandates a highly cryptic lifestyle. This is obtained by living in habitats that are inaccessible, structurally complex, or chemically defended by various forms of camouflage, or by behavior that reduces the chances of detection by predators. Because no single habitat is likely to provide both optimal food and optimal shelter, SCs must either choose long-term habitats and trade food for shelter or shuttle between habitats. Habitat use will of course be constrained by the tolerance of individual SCs to variation in environmental factors like water motion, sedimentation, temperature, salinity, desiccation and oxygen concentration. SCs often need to move in order to avoid environmental extremes, or to find mates, food or free space. This movement occurs over a wide range of spatial scales, both passively and actively. Active movement often occurs at night in an apparent attempt to avoid predatory fishes. Improving our knowledge of the natural history of SCs will be critical to further elucidating the roles that these fascinating but often overlooked animals play in the functioning of benthic ecosystems.

INTRODUCTION Coverage This chapter considers free-living estuarine and coastal benthic crustaceans up to about 20 mm long. A  wide range of taxonomic groups are represented in the small free-living crustaceans (SCs), but I focus on the most common and best known ones: amphipods, isopods, tanaids and

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Small Free-living Crustaceans Gammarid amphipod

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10 mm Sphaeromatid isopod 0.1 mm

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Fig. 9.1. Representative examples of small free-living crustaceans; scale bars are 1  mm long unless otherwise stated. From Hobson and Chess (1976), with permission from Fishery Bulletin; McLay (1988), with permission from C.L. McLay; and Howard and Edgar (1994), with permission from Pearson.

cumaceans (Peracarida), crabs and caridean shrimps (Decapoda), harpacticoid copepods, and ostracods (Fig. 9.1). I  mention only briefly those with lifestyles covered in specialist chapters elsewhere in this volume (e.g., planktonic, freshwater, hermits, symbiotic, semisessile (especially burrowers), deep-sea, etc.). Importance of SCs SCs are ubiquitous in benthic habitats worldwide and are often the numerically dominant macrofauna (Brawley 1992, Cowles et al. 2009). In the few habitats where the productivity of SCs has been compared to that of other organisms, the SCs (and other small mobile invertebrates) dominate the flux of energy and materials through animals in their ecosystem (Edgar and Moore 1986, Taylor 1998a), far outweighing the contribution of more conspicuous and better studied creatures like fishes, sea urchins, and lobsters. The high rate of productivity exhibited by SCs has several important consequences. First, the contribution of SCs to the consumption and production of food makes them an important link between benthic (and sometimes pelagic) primary producers and higher trophic levels such as fishes and shorebirds (Feare and Summers 1986, Jones 1988) and even whales (Oliver et al. 1984). Most small benthic/demersal fishes feed mainly or exclusively on SCs until they reach about 100 mm in length, so SCs are a critical food resource during this stage. Second, SCs are important processors of detritus



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(Vetter 1995)  and regenerators of nutrients (Taylor and Rees 1998). Third, the high rate of productivity exhibited by SCs potentially means they have a strong functional impact on the distribution and abundance of other organisms in their ecosystems. This has been technically difficult to quantify experimentally due to the small size and mobility of SCs, but nonetheless it is becoming increasingly clear that SCs have strong functional impacts on both physical and biological properties of their ecosystem. Meiofauna and amphipods can alter physicochemical properties of soft sediments through bioturbation and tube building (Mills 1967, Ciarelli et al. 1999), and tube-building species can also alter the physical appearance of hard-bottom habitats by forming dense mats (Sebens 1986). SCs can exclude other SCs and larger organisms by consuming them or their larvae, or by outcompeting them for food or space (Conlan 1994). Impacts on biogenic habitat, such as macrophytes and corals, can be negative if the SCs are consuming their host directly or positive if they are removing other organisms that prey upon or compete with their host (Duffy 1990, Stachowicz and Hay 1999a). In the most dramatic case, herbivorous SCs unconstrained by predators can destroy seaweed forests over large areas (Kangas et al. 1982, Tegner and Dayton 1987). Major Challenges Obtaining Food Virtually all forms of particulate organic matter in their environment can potentially be utilized by SCs and dietary specialization is rare, but constraints on habitat use preclude many options. There is evidence of food limitation in macrophyte-associated communities, where individuals feed mainly on epiphytic microalgae and are limited by its productivity (Edgar 1993). Food limitation is potentially widespread in other habitats but is difficult to demonstrate. Avoiding Predation Most SCs have no protective shell, are not chemically defended, and have a high protein content, making them ideal foods for small to medium-sized predators. Most benthic/demersal fishes (including species that are herbivorous as adults) begin their post-settlement life on a diet of copepods, shift to peracarids when they reach about 20–30 mm body length, then eat small decapods at about 100 mm, so the whole range of animals covered in this chapter are potential prey. Shorebirds and gray whales are capable of consuming vast numbers of soft sediment-dwelling crustaceans (Oliver et al. 1984, Hamilton et al. 2006). Within the SC guild, small decapods, such as shrimps and crabs, can be important predators of smaller SCs, such as amphipods (Nelson 1979, Marx and Herrnkind 1985), and cannibalism occurs in some groups. Other predators include nemerteans, polychaetes, leeches, and priapulids (Conlan 1994). Larger individuals and those moving about actively (such as males searching for mates) are often particularly vulnerable to predation (Sudo and Azeta 1992). Unsurprisingly, predator exclusion experiments run in the field or in mesocosms generally show a very strong effect of predation on SCs (e.g., Duffy and Hay 2000, Hamilton et al. 2006). In addition to removal via direct consumption, predators may reduce the fitness of SCs by reducing the feeding rates of individuals, which can translate into reduced growth at the population level (i.e., sublethal or “nonconsumptive” effects). Such effects have been demonstrated for amphipods that were exposed to cues from predatory fishes prevented from physically attacking them (Pérez-Matus and Shima 2010, Reynolds and Sotka 2011). Another way in which larger consumers can negatively affect SCs without necessarily eating them is when sea urchins and

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Small Free-living Crustaceans herbivorous fishes remove biogenic habitat, such as macrophytes. This habitat can be critical for SCs that have no diapause (resting) stage in their life cycle and thus depend on their habitat for food and shelter year-round. Coping with Physical Conditions Most of the world’s seafloor is a relatively stable environment where violent water movement is minimal and variation in physicochemical factors is moderated by the resistance to change of the oceans’ massive water volumes. SCs living in deeper subtidal habitats therefore are able to become well-adapted to a narrow range of environmental conditions. However, where shallow marine environments are exposed to wave action, atmospheric influences, or freshwater runoff from land, physical disturbance and fluctuations in variables such as temperature and salinity create serious challenges for SCs and other organisms (Vernberg and Vernberg 1972). Thus, as might be expected, the core requirements of food and shelter from both predation and environmental stressors lead to SCs being most abundant in structurally complex habitats (Hicks 1986, Taylor and Cole 1994), where food is plentiful, predation is weak, and the physical environment is relatively benign. Responses to optimal combinations of these factors can be spectacular, as shown by very high densities of suspension feeders like caprellid amphipods in strong currents on isolated mooring ropes and other artificial structures, and enormous numbers of detritivorous amphipods in macrophyte accumulations on beaches (Cowles et al. 2009) and in submarine canyons (Vetter 1995). In a survey of common coastal habitats around northern New Zealand, the highest abundance of SCs occurred in coralline algal turf and under beach-cast seaweed (wrack), both structurally complex habitats providing shelter from predators and environmental stressors and containing plentiful food (Fig. 9.2; Cowles et al. 2009). Movement Movement on various temporal and spatial scales is frequently necessary to find mates (Forbes et al. 1996) and food, and emigration to new habitat may be necessitated by competition for food or space, physical and biological disturbance (Conlan 1994), or environmental extremes (Fish and Fish 1978). Rapid directed movement is integral to the lifestyles of scavenging SCs that utilize ephemeral food resources such as incapacitated fish and lobsters (Sekiguchi 1982, Stepien and Brusca 1985), animals exposed by physical disturbances caused by whale feeding (Oliver and Slattery 1985), or algal detritus (Edgar 1992). Over longer time scales, dispersal is also critical for many tube-building amphipods, which are weak competitors for space and so rely on rapid colonization of cleared surfaces before they are eventually displaced by sessile organisms (Sebens 1986). Long-distance dispersal may be particularly problematic for those SCs that have no pelagic larval stage, such as peracarids (amphipods, isopods, tanaids, and cumaceans; Johnson et al. 2001), ostracods (Cohen and Morin 1990), and most harpacticoid copepods (Hicks and Coull 1983), although adults of some species can disperse widely by rafting on floating objects (Thiel and Haye 2006). Limited dispersal can lead to inbreeding in potentially isolated habitats like high-shore rockpools (Hicks and Coull 1983) and seaweed holdfasts (Thiel and Vásquez 2000), thus generating an additional motivation to disperse. Dispersal can be detrimental. Dispersing individuals risk the failure to find a mate, suitable habitat, or food, whereas SCs that disperse by swimming expose themselves to predators in the water column (Conlan 1994). Even “successful” dispersal to apparently suitable habitat can result in the loss of local adaptation. Over very small spatial scales, local Tigriopus californicus (a harpacticoid copepod) perform better reproductively than those from nearby tidepools (Brown 1991). The



Richard B. Taylor

A

Subtidal coralline turf Sheltered seaweed wrack Carpophyllum plumosum Shell hash Moderate seaweed wrack Intertidal coralline turf 5 m deep sand 10 m deep sand Ecklonia radiata fronds Exposed low sand Perna canaliculus Sandflat Sheltered mid sand Seagrass sediment 20 m deep sand 2 m deep sand Ecklonia radiata holdfast Rhodophytes Mangrove mud Urchin barrens Moderate low sand Seagrass blades Mudflat Sheltered high sand Sheltered low sand Moderate mid sand Exposed high sand Limnoperna pulex Moderate high sand Exposed mid sand Channel hash Atrina zelandica Pneumatophores Bare rock

B

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Subtidal rocky reef Subtidal soft sediments Intertidal sandy beach Intertidal rocky reef Estuary

Density (ind. m

−2)

Fig. 9.2. Densities of small (0.5–8  mm) mobile crustaceans in a wide range of coastal habitats in northeastern New Zealand at (A) fine-scale and (B) broad-scale habitat levels. Bar patterns in (A) match those in (B). Bars represent averages (+ 1 SE). Data from A. Cowles, see Cowles et al. (2009) for details of methods.

relative costs and benefits of dispersal will depend on the balance of many factors, likely varying in space and time (Franz and Mohamed 1989). Fouling Another important challenge is resisting fouling of the exoskeleton, gills, sensory structures, and eggs (Fernandez-Leborans 2010, Bauer 2013). Common foulants are sessile organisms requiring a substratum, parasites seeking a host, and fine sediment particles settling passively. However, fouling is occasionally advantageous when it helps with camouflage (Fernandez-Leborans 2010).

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WHAT IS KNOWN? Obtaining Food Collectively, SCs consume most forms of particulate organic matter available in benthic habitats. Diets of most species of SCs are broad, with dietary specialization far rarer than in the insects, the main group of terrestrial arthropods (Hay and Steinberg 1992). To illustrate the dietary range of some SCs, the caprellid amphipod Paracaprella tenuis can filter fine particles from the water column, grasp larger moving prey like copepods, scrape unicellular organisms such as diatoms from benthic substrata, and scavenge carcasses of small animals (Caine 1974). As another example, the idoteid isopods Idotea balthica and I. emarginata mainly eat dead or dying parts of brown seaweeds, but also consume animal carrion and small live animals, including juveniles of their own species, and will even take swimming Artemia nauplii in aquaria (Franke and Janke 1998). Crustaceans use a wide range of appendages for feeding. These are reviewed elsewhere (McLaughlin 1982, Grahame 1983) and are covered in detail in Volume One (Watling 2013), so will not be covered here. Host Organisms Living macrophytes such as seaweeds and seagrasses are often the most conspicuous potential foods for SCs, and individuals of many species are able to graze epidermal tissue off their host macrophyte (see detailed account in Chapter 18 of this volume). Animal hosts such as gorgonians may also be consumed (Scinto et al. 2008). Microorganisms Microalgae, either single-celled like diatoms, or multicellular, are abundant on submerged surfaces like macrophytes (Hicks 1986)  and sediments (Cahoon and Cooke 1992). Epiphytic algae can be half as productive as their host macrophyte (Borum and Wium-Andersen 1980)  and of greater nutritional value because they typically lack structural materials and secondary metabolites and have higher protein contents (Klumpp et al. 1992). The algae appear to dominate the diets of most phytal SCs (Edgar 1993) and are often preferred over the host (Bell 1991). In soft sediments, microalgae are a major food source for amphipods like Corophium volutator (Gerdol and Hughes 1994). Bacteria are eaten by small SCs, like harpacticoid copepods, and by larger detritivorous SCs (Nielsen and Kofoed 1982, Hicks 1986). Detritus Detritus can be the dominant food in environments that are too dark or too physically unstable to support primary producers, and most macrophyte production is thought to enter aquatic food webs as detritus following microbial colonization and transformation rather than being eaten directly. SCs are capable of consuming all size classes of detritus, from tiny particles of organic matter picked out of soft sediments by harpacticoid copepods and amphipods (Nielsen and Kofoed 1982, Hicks and Coull 1983) to thick mats of whole detached seaweed plants set upon by a dedicated guild of amphipods and leptostracans (Vetter 1995). Many “detritivores” actually derive most of their nourishment from microorganisms coating the detritus (Hicks and Coull 1983).



Richard B. Taylor

Suspended Particles Suspension feeding involves the extraction of small organic particles (both living and dead) from the water column. Because these particles are usually generated elsewhere (e.g., in pelagic habitats) and are constantly delivered via physical mechanisms like tidal currents, they remove the dependence of SCs on in situ production and allow them to reach extremely high densities. Suspension feeding amphipods (ischyrocerids, podocerids, and caprellids) often dominate in areas of high water motion (Edgar and Moore 1986). Less spectacular, but probably of more widespread importance, is the ability of soft sediment-dwelling SCs like amphipods of the genus Corophium to filter very small particles including bacteria from still water (Fenchel et al. 1975, Shillaker and Moore 1987, see also Chapter 15 in this volume). Animals Predation, the consumption of other animals, is the final major feeding mode. Items available to predatory SCs are other small mobile invertebrates including early life stages of larger animals (Conlan 1994), large mobile animals like echinoderms, and various sessile animals (Schnabel and Hebert 2003). Predation by SCs may be more common than previously recognized because several species previously thought of as herbivores are now known to eat live prey (Franke and Janke 1998, Dick et al. 2005). Maximizing Food Intake SCs locate food using a highly developed sense of smell, detecting chemical cues such as specific amino acids using receptors on the antennae and possibly other appendages (Bauer 2004, Thiel 2011). Modeling of arrival times at bait suggests deep-sea amphipods can detect carrion from up to 2 km away (Sainte-Marie and Hargrave 1987). SCs can increase the quantity and/or quality of food they ingest through behavioral means. For example, suspension feeders like the gammarid amphipod Ericthonius punctatus and certain arcturid isopods maximize their access to particles in the water column by climbing to the top of any available projection (Barnard et al. 1988, A. Maywald personal observation, in Debelius 2001). Another podocerid amphipod, Dyopedos porrectus, builds “whips” on its hydroid host from sediment particles, which it climbs up, again apparently to increase access to the water column for suspension feeding (Moore and Earll 1985, Mattson and Cedhagen 1989). A third podocerid, Dulichia rhabdoplastis, builds rods on sea urchin spines out of feces and inorganic particles and feeds on suspended material from them in the winter like D. porrectus, but during the summer it uses them as a substratum for “farming” diatoms (McCloskey 1970). Other SCs target high-quality food on fine spatial scales; for example, the gammarid amphipods Tethygeneia sp. and Protohyale rubra preferentially eat subapical meristematic tissues of the brown seaweed Zonaria angustata, which contain few phlorotannins, phenolic secondary metabolites thought to reduce palatability or digestibility (Poore 1994). Interference competition for food and/or space can occur in dense populations; for example, individuals of the gammarid amphipod Ericthonius punctatus maintain feeding territories of a body-length radius around their tube, from which they exclude conspecifics (Connell 1963), whereas larger individuals of E. punctatus (mentioned earlier) competitively dominate smaller ones by climbing over them to obtain better access to particles in the water column (Barnard et al. 1988). The suspension-feeding porcelain crab Petrolisthes cinctipes also occurs abundantly in patches due to gregarious settlement and competes for food at high densities, with small individuals suffering most (Donahue 2004).

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Small Free-living Crustaceans The effects of intermittent food limitation may be reduced through life history adaptations. The idoteid isopod Idotea metallica lives on floating objects in oligotrophic waters, so is likely to have to deal with frequent periods of food limitation. It can withstand short-term experimental starvation with few consequences, at least in part by utilizing stored lipid, whereas its congener I. balthica has a relatively constant food supply in nature (seaweeds growing in large beds on the rocky shore) and is affected far more by experimental starvation (Gutow et al. 2006, 2007). Avoiding Predation Predation is likely one of the strongest selective pressures on SCs. There are a number of ways in which SCs reduce their exposure to predators. Habitat Use The most obvious way to avoid predation is to live in a microhabitat that is inaccessible to common predators, such as rock crevices (Hines 1982), high intertidal rock pools (Dethier 1980), or biogenic habitats such as seaweed holdfasts, branching corals, sponges, and mussel clumps (e.g., Thiel and Dernedde 1994). Protective microhabitats “engineered” by individual SCs or commandeered from other organisms include tubes and burrows in soft sediments (see Chapter 3 in this volume). Where predators have physical access to habitats, structurally complex ones usually confer greater protection from predators than do simple habitats such as flat-bladed seaweeds (Hicks 1986). Structurally complex habitats are presumed to be more difficult to search for prey than are simple habitats with the same surface area. However, there are exceptions, as when a large individual is exposed on a narrow substratum (Stoner 1982, Edgar 1983, Holmlund et al. 1990). Where macrophyte-associated SCs are subject to predation from omnivorous fishes, incidental consumption by herbivorous fishes, or destruction of their host organism by fish or sea urchins, an “associational defense” may be gained from living on macrophytes that are unpalatable to the larger consumers (Hay et al. 1987). Of course, optimal food and optimal refuge from consumers are not always found in the same microhabitat. Mark Hay and Emmett Duffy et al. have argued that the consequent trade-off leads to selective pressure to inhabit and eat foods that are distasteful to larger consumers (Hay et al. 1987, 1988). Support for this hypothesis has come from studies in a number of regions (Hay 1992). The principle was expanded to chemically defended animal hosts in an interesting study showing that the amphipod Pleusymtes symbiotica gains a refuge from fish predation while on the octocoral Melithaea flabellifera (Kumagai 2008). In this example and others (Boström and Mattila 1999, Lasley-Rasher et al. 2011), the refuge value of the host to SCs apparently outweighs its value as a food source because the SCs prefer to eat other food items. The aforementioned studies have each been done on only one or a few arbitrarily chosen SC species, which may not be representative of other host-associated SCs, and the implicit prediction that SCs would be more diverse and/ or abundant on hosts that are unpalatable to larger consumers was not supported in the one system where this has been tested (Australasian rocky reefs; Taylor and Steinberg 2005). In Idotea balthica, the trade-off changes with sex and age (Merilaita and Jormalainen 2000) and even time of day (Vesakoski et al. 2008). The distributional patterns listed here could be generated by either (i)  active selection of safe substrata by SCs, (ii) nonselective habitation of substrata followed by differential predation, or (iii) a combination of both. Some SCs can distinguish structurally complex substrata from simpler forms that offer less protection (Hansen et al. 2011), but this important issue requires more research.



Richard B. Taylor

Camouflage Because many or most predators of SCs are visual feeders, camouflage can help SCs avoid detection. There are a number of ways in which they achieve this. Color Color matching the background minimizes visual contrast (Cott 1940). Many SCs do this using different colored chromatophores and/or pigments such as carotenoids (McNamara and Milograna, 2015). In crustaceans, chromatophores are under hormonal control, so do not respond to stimuli as quickly as the neurally controlled chromatophores of animals such as cephalopods and chameleons; but, nevertheless, chromatophores can radically alter the overall color of crustaceans. This occurs on the scale of minutes by dispersing or concentrating individual chromatophores, or over days to weeks by changing the number of chromatophores (Bauer 2004). Pigments from food sources such as algae are incorporated (with modification) into the exoskeletons of some crabs and isopods, but although these enable very accurate color matching to seaweed hosts, major color changes require molting, so this method best suits species that rarely or never change hosts (Lee and Gilchrist 1972, Hines 1982). Camouflage can also be acquired from other organic and inorganic objects. This is done by the decorator crabs of the superfamily Majoidea, which attach parts or all of individual sessile organisms to their dorsal carapace using hooked setae (Hines 1982). The incidence of decorating is usually highest in young crabs, presumably because they are the most vulnerable to predators and/or because camouflage is less effective for larger individuals (Hultgren and Stachowicz 2009). Crabs of several other families carry objects above their carapace using the rear pereopods (Wicksten 1986, Guinot et al. 1995). Similarly, the tubes of gammarid amphipods such as Microdeutopus gryllotalpa are thought to act as camouflage against visually feeding fishes (Borowsky 1983). Transparency is a passive means of color matching, requiring clear tissues and the absence of pigmentation in the exoskeleton, and although most developed in planktonic organisms, it is also common in caridean shrimps (Bruce 1975, Wicksten 1983, Bauer 2004). Disruptive coloration breaks up an organism’s outline and makes characteristic features indistinct without the organism as a whole necessarily blending into the background (Cott 1940). It has the major advantage of working across a variety of backgrounds (Merilaita 1998) and may be used in conjunction with background color matching by fine-tuning with chromatophores ( Jormalainen and Tuomi 1989). Disruptive coloration is apparently used by the caridean shrimp Heptacarpus sitchensis, which actively wanders over varied substrata and does not attempt to color-match its background, as opposed to the more sedentary Hippolyte varians, which stays on single substrata for much longer and does color-match its background (Bauer 2004). There is strong evidence for disruptive coloration in certain color morphs of Idotea balthica, which have more spots located on margins of the body (serving to break up the animal’s outline) than would be expected by chance (Merilaita 1998). The eye is highly conspicuous in many organisms and is often disguised by means of stripes and other disruptive means (Cott 1940). The arcturid isopod Astacilla longicornis purportedly increases its camouflage on the sea pen Funiculina quadrangularis by concealing its large eye using structures unrelated to vision (Nilsson and Nilsson 1983). Individuals of some species assume disruptive coloration patterns as they grow, after color-matching their background when juveniles (e.g., the caridean shrimps Latreutes fucorum and Hippolyte coerulescens; Hacker and Madin 1991). Some species of harpacticoid copepods (Battaglia 1958), brachyuran crabs (Hines 1982), caridean shrimps (Bauer 2004), and sphaeromatid and idoteid isopods (Holdich 1969, Salemaa 1978) have multiple distinct color morphs (18 in the extreme case of juveniles of the brachyuran crab Cancer productus; Krause-Nehring et al. 2010). Color polymorphism is thought to reduce susceptibility to visually feeding predators, principally because predators struggle to simultaneously

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Small Free-living Crustaceans form search images of more than one color morph (Cott 1940). The morphs often have a genetic basis (Hedgecock et al. 1982), and the relative frequencies can cycle through time as selection pressure always favors the least abundant one (Bauer 2004). In larger crustaceans, color polymorphism often disappears as individuals age, with adults being monochromatic (Palma and Steneck 2001, Todd et al. 2009, Krause-Nehring et al. 2010). Shape-matching Matching of an organism’s morphology to its substratum also increases crypsis and can be extremely effective, especially when used in conjunction with color matching. For instance, some caridean shrimps accurately mimic the shape and color of seaweed vesicles or fronds and inhabit those parts of the seaweed that they best match (Hacker and Madin 1991). The body of Hippolyte coerulescens “is banded with brownish yellow in such a way that it seems to be broken up into two parts, each of which looks very like a vesicle of Sargassum” (Gurney 1936; Fig. 9.3). The crab Thersandrus compressus mimics the felty surface of its exclusive host, the tropical green seaweed Avrainvillea longicaulis, so accurately that the crab is very difficult to locate in the field, and it is usually only noticed in the lab after being accidentally sampled along with the seaweed (Hay et al. 1990a). Bumps and other projections on the carapaces of small crabs can make them very difficult to distinguish from irregular hard-bottom substrata, especially when they tuck their legs under the carapace (Wicksten 1983). Defenses Structural defenses, such as spines or a thickened carapace, appear to be relatively rare in SCs, although a very high incidence of spines and humps on low-latitude idoteid isopods has been considered an evolutionary response to intense fish predation (Wallerstein and Brusca 1982). Ostracods are another exception because their bivalved shell can confer sufficient protection to allow them to pass through fish guts unharmed (Vinyard 1979). It is likely that the ability of sphaeromatid isopods to roll into tight balls protects them against some predators, but I have been unable to find any evidence for this. Objects in the environment may be employed as structural defenses. Empty gastropod shells are used, presumably for defense, by some tanaids (Messing 1983), and several gammarid amphipods (Carter 1982) and the gammarid amphipod Atylus collingi possibly uses shell fragments as a portable shelter (Oliver and Slattery 1985). Induction of diverse structural defenses in response to the presence of predators occurs in planktonic freshwater cladocerans (Tollrian and Dodson 1999) and barnacles (Lively 1986), but to my knowledge this has not been observed in small mobile benthic crustaceans. Although not a free-living crustacean, the hermit crab Pagurus filholi almost qualifies as having an inducible structural defense, choosing more protective shells in the presence of predators (Mima et al. 2003). Chemical defenses are also rare in SCs, but there are a few interesting cases. Some gammarid amphipods appear to have chemically defended tissues; for example, Paradexamine fissicauda (Amsler et  al. 2013), Chromopleustes spp. and Cryptodius kelleri (Norton and Lindquist 1999, Shimek 2004), and Amaryllis philatelica (Lowry and Stoddart 2002). Paradexamine fissicauda sequesters halogenated secondary metabolites from the red alga Plocamium cartilagineum, which reduces the amphipod’s palatability to fishes (Amsler et al. 2013), and Shimek (2004) suggests that Chromopleustes spp. may sequester saponins from sea cucumbers. Juveniles of the idoteid isopod Idotea emarginata appear to release a distasteful chemical that prevents their consumption by larger isopods (Franke and Janke 1998). Santia spp. isopods are protected against predators by metabolites produced by symbiotic bacteria on their exoskeleton (Lindquist et al. 2005). Behavioral sequestration of chemical defenses is shown by the amphipod Pseudamphithoides incurvaria, which wraps



Richard B. Taylor

Fig. 9.3. The caridean shrimp Hippolyte coerulescens on floating Sargassum sp., a brown seaweed. The shrimp’s coloration and body form closely resembles the seaweed’s vesicles. From Gurney (1936), with permission from Wiley.

a piece of chemically defended seaweed around itself (Hay et al. 1990b), and by crabs of various families that attach chemically defended organisms to their carapace (Wicksten 1986, Guinot et al. 1995, Stachowicz and Hay 1999b). Small xanthid crabs of the subfamily Polydectinae (the “boxer” crabs) carry a stinging sea anemone in each cheliped (Karplus et al. 1998). A few SCs appear to mimic unpalatable or poisonous animals (Batesian mimicry), using a combination of color, morphology, and behavior. The best-known examples are between gammarid amphipods (the mimics) and small gastropods (the models): Pleustes platypa and Mitrella carinata (Crane 1969), Stenopleustes spp. and Lacuna spp. (Field 1974), and Podocerus sp. and Flabellina trilineata (Goddard 1984). In an aquarium experiment, Stenopleustes were less vulnerable to fish than were a nonmimetic amphipod (Field 1974). Markings on several species of caridean shrimps and brachyuran crabs have been interpreted as “eye-spots” or ocelli (Bruce 1975, Debelius 2001),

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Small Free-living Crustaceans but there is no evidence that predators recognize them as such, let alone that they are intimidated by them or deflect strikes toward them in the way that some terrestrial predators may respond to eye-spots (Cott 1940, Stevens 2005). Behavioral Responses to Predators “Immediate” Responses Because avoiding predation often incurs costs in terms of lost opportunities to seek optimal food or mates, it should be advantageous for SCs to be able to recognize predators when they are nearby so that they can engage in other activities when predators are absent. A number of SCs have now been shown to be able to detect and respond to cues from predators or wounded prey (Main 1987, Hazlett 2011, Thiel 2011). There are a number of behaviors that SCs can use to reduce their chances of detection. (a) The first is to spend more time in relatively safe microhabitats. In the presence of predatory fishes, the seagrass-dwelling shrimp Tozeuma carolinense moves from near the seafloor to the dense seagrass canopy where fish tend not to forage (Main 1987), and the microhabitat preference of the isopod Erichsonella attenuata switched from one with food to one with shelter when fish were introduced (Boström and Mattila 1999). (b) Moving prey are more susceptible to fish, so stillness can be advantageous (Caine 1989a, 1991). Tozeuma carolinense moves less in the presence of fishes, increasing the time it spends clinging to seagrass blades at the expense of time spent feeding (Main 1987), and male amphipods spend less time on the sediment surface looking for females when birds are present (Conlan 1994). (c) Elongate SCs, such as idoteid isopods and some shrimps that inhabit narrow-bladed macrophytes, align their bodies parallel to their host ( Jones 1971, Main 1987). This undoubtedly helps the animals grip their substrata as well as making them less conspicuous to predators, but the shrimp T. carolinense goes further by moving to the opposite side of its seagrass blade when a fish approaches, so that only its eyestalks are visible (Main 1987; Fig. 9.4). In a laboratory study, juvenile penaeid shrimps went further still by recognizing whether nearby fish were actively hunting or satiated; the shrimps responded to the former by lying parallel along mangrove pneumatophores but ignored the latter (Primavera 1997). (d) Finally, burial in sediments is used by many crabs to avoid predators (Bellwood 2002). There are a variety of responses to attack. (a) Many SCs are capable of short bursts of speed to evade predators. The tail flick of caridean shrimps generates a very rapid backward movement in response to attempted predation, with 40% of the total mass of the shrimp dedicated to muscle powering this rare maneuver (Meyhöfer and Daniel 1990). (b) Crabs sometimes escape from predators by nipping their attacker with their chelipeds, prompting their release (Wasson and Lyon 2005). (c) Some crabs and isopods hold on to the substratum very tightly when threatened, making themselves more difficult to detach and consume (Hines 1982). (d) When physically contacted, the small brachyuran crab Heterozius rotundifrons assumes a rigid catatonic posture with chelipeds outspread, causing predatory fishes to release it (Hazlett and McLay 2000). (e) Limb autotomy, the deliberate casting off of a limb through self-amputation, is an effective defense against predators that grasp walking legs and chelipeds as part of the capture process ( Juanes and Smith 1995, Wasson et al. 2002). Limb autotomy is known in decapods and isopods (Charmantier-Daures and Vernet 2004), and it presumably also occurs in other “lower” crustaceans. It is an expensive last resort, with autotomized legs normally taking a few molts to regenerate fully (Brock and Smith 1998). Timing Activity to Avoid Predators In an apparent attempt to minimize their exposure to visual predators, a diverse range of SCs inhabit refugia such as soft sediments, coral, and macrophytes by day and emerge at night



Richard B. Taylor

Fig. 9.4. Predator avoidance behavior in the seagrass-dwelling caridean shrimp Tozeuma carolinense. The sequence shows a shrimp moving to the opposite side of a seagrass blade from a predatory fish, with an extended eyestalk visible in the final photograph. From Main (1987), with permission from the Ecological Society of America.

to feed and find mates (Fig. 9.5). Those that spend time swimming in the water column are termed “demersal zooplankton” (Hammer 1981). For example, some gammarid amphipods live on chemically defended seaweeds by day and move onto palatable ones at night to feed (Buschmann 1990, Aumack et al. 2011). In these cases, the defended seaweeds apparently compensate for their inedibility by comprising a good refuge. The strategy of sheltering during the day to avoid predators and seeking food at night has been suspected in amphipods for nearly a century (Blegvad 1922, cited in Williams and Bynum 1972). Nocturnal movement does not allow SCs to completely avoid predators because nocturnal fishes can still take a heavy toll (Sudo and Azeta 1992), and some SCs avoid moonlit nights, presumably to reduce their exposure further (Alldredge and King 1980). In summary, the (few) SCs that are conspicuous during daytime in the presence of predators are likely to be chemically defended, mimics of defended species, or living on a defended organism. Coping with Physical Conditions The consequences of physical “disturbance” must be viewed relative to the needs and tolerances of individual organisms because something like strong water movement or warmth may be a debilitating stressor for one organism but a fundamental requirement for another. Disturbance also needs to be considered at the level of both the individual and the population. For instance, a disturbance may have a lethal impact on affected individuals without any significant local population-level consequences if replacement is rapid (for example via immigration from unaffected areas).

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Day

Night

Fig. 9.5. Day–night differences in the distribution of seagrass fauna. From Howard and Edgar (1994), with permission from Pearson.

Wave Action Wave action generates massive drag forces on organisms in exposed shallow-water habitats (Denny 1988). Although their small size may provide some protection within the boundary layer of still water surrounding all aquatic objects, drag can potentially cause SCs to be dislodged from their habitat or for their substratum to be dislodged along with them (e.g., when unconsolidated sediments are resuspended or biogenic habitats such as macrophytes are torn loose from the seafloor). Less dramatically, the disturbance caused by wave action can reduce feeding rates of SCs (Engkvist et al. 2004). Responses to wave action vary among SCs. Biomasses of soft-sediment animal communities are negatively correlated with wave exposure (Ricciardi and Bourget 1999), perhaps because of the physical instability of this habitat and the resultant abrasion and lack of stable substrata. However, the abundance of phytal fauna is often highest at wave-exposed sites (Fenwick 1976). For these animals, the stress imposed by the physical force is clearly offset by the associated advantages, which



Richard B. Taylor

probably include the provision of food for suspension feeders, the removal of silt, and/or the inhibition of predation. Animals in soft sediments exposed to strong water movement (e.g., swash zone of beaches) use burial to avoid displacement (Giere 2009). SCs living in hard-bottom habitats have a number of adaptations for resisting dislodgement by wave action. Drag can be minimized by strong dorsoventral flattening (Fig. 9.6), as dramatically exemplified by isopods of the genera Amphoroidea and Plakarthrium and the harpacticoid copepod Porcellidium (Hicks 1986). Gripping the substratum firmly can be achieved in several ways. (a)  Clinging or grasping appendages are often particularly well-developed and robust in SCs inhabiting wave-exposed sites, with animals commonly possessing features such as prehensile pereopods, (Caine 1978) hooked or strengthened dactyls, and “stout spines or cushions of spinules on the proximo-lateral edge of the palm” to oppose them (p.  36, Hicks 1986). Animals in exposed areas also tend to have more robust body somites and appendages (Caine 1989b). (b) Suction mechanisms are present in some harpacticoid copepods (e.g., Porcellidium), with mouthparts and the first pair of thoracic legs modified into a suction cup (Hicks 1986, Gibbons 1991). (c) Mucus adhesion via exudation of polysaccharides is suspected in some harpacticoid copepods (Hicks 1986, Gibbons 1991). (d) The intertidal tube-dwelling tanaid Tanais dulongii spins a “life-line” to tether itself to its algal substratum when crawling in the open, reportedly making it very difficult to dislodge ( Johnson and Attramadal 1982). (e) The effectiveness of these morphological adaptations is maximized by various behaviors. For example, Tigriopus brevicornis, a harpacticoid copepod living in high-shore rock pools, uses small-scale pits in the substratum to anchor various appendages for bracing and gripping in flow (McAllen 2001). Caprellid amphipods alter their stance from upright to parallel with the substratum at wave-exposed sites, presumably to reduce drag (Takeuchi and Hirano 1995). Habitats may be selected at least in part based on their suitability as substrata to cling to in the face of wave action (Nicotri 1980). If the aforementioned adaptations fail, and individuals are dislodged, strong thigmotaxis facilitates rapid reattachment, as seen in Pentidotea montereyensis (Lee 1966). When macrophytes detach from the seafloor, they are likely to be transported to a habitat that is unsuitable for their associated fauna (e.g., deep-sea soft sediments or a sandy beach). In an apparent

5 mm Amphoroidea longipes

1 mm Plakarthrium typicum

0.1 mm Porcellidium sp.

Fig. 9.6. Extreme dorsoventral flattening in two seaweed-dwelling isopods and a harpacticoid copepod. From Wilson et al. (1976), with permission from Wiley; Hurley and Jansen (1977), with permission from NIWA; and Giere (2009), with permission from Springer.

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Small Free-living Crustaceans attempt to avoid this displacement, many macrophyte-associated SCs (and other epifaunal taxa) abandon their host within seconds of its detachment and swim or fall to the seafloor. This obviously creates strong differences between the faunas of attached and recently detached seaweeds, with consequences for the likelihood of long-distance dispersal via floating seaweeds (Kingsford and Choat 1985, Gutow et al. 2009). How macrophyte-associated SCs detect that their host has been dislodged is unknown. Movement of the substratum triggers “bail-out” in various rocky shore mollusks (Shanks et al. 1986, Wright and Shanks 1995) and would also seem a likely prompt for the rapid abandonment of seaweed holdfasts by burrowing limnoriid isopods (Miranda and Thiel 2008). However, movement is a less plausible cue for epifaunal SCs on more distal parts of seaweeds that move constantly in surge while attached. It is possible the SCs see the seafloor receding; their vision up to a meter or so is good enough for them to at least sense dark shapes because many swim toward a diver if he or she is the nearest large object after detaching their host (personal observation). This is supported by the observation that caprellids swim upward to bryozoans on a floating dock when their host bryozoan is detached and begins to sink (Keith 1971). It would be worth testing whether bail-out in SCs occurs in darkness. Incidentally, a diver can exploit bail-out behavior to rapidly evaluate the faunas of different macrophytes in situ by ripping one or two plants off the bottom and observing the magnitude of the subsequent “rain” of animals. Dynamic Sediments Movement of unconsolidated sediments presents a number of challenges to SCs in both hardand soft-bottom habitats. Some sandy beach-dwellers have heavy exoskeletons that may help to resist abrasion from sediment particles (Hayes 1974), as may the ability of sphaeromatid isopods to roll into a tight ball (Bursey and Wooldridge 2003). Agents of disturbance can be biological as well as physical, with the former tending to occur on smaller scales (Hall et al. 1994). For example, the tube-dwelling amphipod Microdeutopus gryllotalpa is excluded from mudflats by the sediment-mobilizing activities of the gastropod Ilyanassa obsoleta (DeWitt and Levinton 1985). On a larger scale, SCs in estuaries and along urban coastlines are vulnerable to smothering or burial when large quantities of terrigenous sediments are deposited following heavy rain (Thrush et al. 2004). Sandflat species vary in their ability to fight their way up through a layer of abruptly deposited sediment (Chang and Levings 1978, Hinchey et al. 2006) and to survive in the new, often sterile, habitat that awaits them if they can reach the surface. In hard-bottom habitats, complex structures such as seaweeds reduce water flow, enhancing the settlement of sediment particles, which accumulate in patches on the bottom and coat the surfaces of the seaweeds in sufficiently calm areas. These deposited sediments enable the existence of characteristic soft-sediment species (Hicks 1986) but may be detrimental to hard-bottom fauna by filling in crevice microhabitats, interfering with feeding and molting, and reducing the productivity of epiphytic algal food items (Hicks 1986). Seaweeds with very high sediment loads thus tend to be occupied by nematodes rather than SCs (Hicks 1986). Turbidity, caused by sediments suspended in the water column, can be detrimental to suspension feeders that eat similar-sized organic particles because they must expend considerable energy to separate this material from the accompanying inorganic matter (Moore 1978). Temperature Like all organisms, SCs perform optimally at a relatively narrow range of temperatures (Panov and McQueen 1998). In the subtidal zone, temperature extremes are usually moderated by the thermal inertia of the oceans, and seasonal cycles are relatively constant across years, although



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additional variation may be imposed by large-scale phenomena, such as El Niño/La Niña cycles, and small-scale phenomena, such as upwelling and input from major rivers. In the intertidal zone, temperature fluctuations are much larger and less predictable due to the influence of the atmosphere. Some intertidal crustaceans can tolerate temperature extremes including freezing (McAllen and Block 1997, Drolet et al. 2013), whereas others either succumb or undergo seasonal migrations to less stressful environments, such as under large rocks or in the subtidal zone (Steele 1976, Fish and Fish 1978, Skadsheim 1983, Thiel and Dernedde 1994). Salinity Salinity is very stable in most subtidal habitats but varies greatly in estuaries and rock pools, creating a major physiological challenge for resident SCs. In estuaries, salinities can range from zero to full strength seawater within a tidal cycle, whereas high rock pools may contain pure freshwater after heavy rain or become hypersaline after dry periods with calm seas. The thin exoskeletons and exposed gills of SCs make it very difficult for them to resist osmotic pressure from surrounding waters that do not match their internal solute concentrations, so most can osmoregulate over a fairly limited range before they osmoconform (Beadle 1972). Like other organisms, SCs in soft sediments can obtain a refuge from salinity extremes by burrowing into sediments, where salinity changes in the overlying water are greatly moderated (Sanders et al. 1965). Desiccation Desiccation can be deadly in the intertidal, especially toward the top of the shore where emersion times are longest. Most SCs are physiologically vulnerable to desiccation due to their relatively thin and water-permeable exoskeletons. The effects of desiccation at low tide can be minimized behaviorally. At low tide the mid- to high-shore sphaeromatid isopod Campecopea hirsuta seals off its desiccation-prone pleopods and other ventral surfaces by rolling itself into a tight ball and is thus able to survive long periods exposed to dry air (Fig. 9.7; Wieser 1963). In contrast, the low-shore isopod Ulva bidentata is unable to form a similarly tight ball and dehydrates rapidly in dry air (Wieser 1963). Other SCs seek damp microhabitats within the intertidal or retreat to the subtidal zone. For example, when the high intertidal rock pools it inhabits dry out, the harpacticoid copepod Tigriopus brevicornis survives inside water-filled tubes of the green seaweed Ulva intestinalis or in damp soft sediments (McAllen 1999, 2001). The harpacticoid Porcellidium sp. migrates down into the damper basal parts of its host seaweed at low tide, especially during daytime when desiccation stress is greater than at night (Gibbons 1989). Amphipods from the genus Hyale shelter in seaweeds (Beckley 1980)  or beneath limpets (Underwood and Verstegen 1988). The tube-dwelling tanaid Tanais dulongii retains water in its tube at low tide ( Johnson and Attramadal 1982). Other animals completely move out of the intertidal zone at low tide. On intertidal seaweeds, the abundance of various SCs decreased at low tide, with the animals inferred to move into the lower intertidal or subtidal zone (Wieser 1952, Davenport et al. 1999). However, emigration was weakest in coralline turf fauna; their host seaweed retained water better than the other species examined (Davenport et al. 1999). In soft sediments, harpacticoid copepods move several centimeters down into the sand at low tide, then return to the surface at high tide (Little 2000). In the supralittoral zone of sandy beaches, where tidal inundation is rare and the sand well-drained, highest abundances of animals are found in seaweed wrack and the moist sand beneath it (Cowles et al. 2009).

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A

B

1 mm 1 mm

C

juv. 1 mm

Fig. 9.7. Positions assumed by two sphaeromatid isopods when exposed to dry air. The low-shore Dynamene bidentata (A, male and B, female) rapidly dehydrates in dry air due to water loss through its exposed gills, whereas the mid- to high-shore Campecopea hirsuta (C, juvenile male) is able to form a tightly sealed ball and can resist desiccation for much longer. Drawing by M. Wimmer, from Wieser (1963), with permission from Journal of the Marine Biological Association of the United Kingdom.

Oxygen Oxygen availability plays a major role in the life of soft-sediment dwelling SCs because oxygen in pore water is removed through respiration and replaced very slowly through diffusion, such that fine sediments (clays and silts) are anoxic a few millimeters below the surface. Exceptions occur where bioturbators irrigate the sediment, and there may be localized oases of oxygen around burrows or macrophyte roots. Coarser sediments are much better ventilated, so the anoxic layer is deeper (Little 2000). In hard-bottom habitats, oxygen can become depleted within dense algal tufts at low tide and at night due to respiration (Wieser and Kanwisher 1959, Pöhn et al. 2001) or supersaturated during the day due to photosynthesis (Pöhn et al. 2001). Supersaturation can lead to the production of toxic hydrogen peroxide (Abele-Oeschger et al. 1994). Both hypoxic and hyperoxic conditions have been suggested to trigger emigration of fauna (Wieser and Kanwisher 1959, Pöhn et al. 2001).



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The idoteid isopod Idotea emarginata is more tolerant of anoxia than its congener I. balthica, which correlates with the habitats of these two species: I. emarginata occurs in hypoxic decaying algal mats whereas I. balthica lives in normoxic floating mats of living algae (Vetter et al. 1999). Ultraviolet Light Ultraviolet (UV) radiation (2 years

2–10 cm

Examples Krill

1–2 years 5–20 mm 2–5 mm 1–2 mm 12 months). Crayfish are known to actively seek new sites during specific periods of their life histories when conditions favor relatively long-distance movements over short-term movements. Other inland crustacean species can disperse to distant islands as larvae carried by oceanic currents, and many have drought-resistant stages during their life histories that enhance aerial dispersal by birds and other animals (e.g., Covich 2006, Hawes 2009, MacKay and Williams 2011). Certain species can also actively colonize continental lakes and ponds by moving among interconnected freshwater habitats (streams, ponds, lakes, and wetlands) linked by drainage networks. The long-term spatial distribution of these species can reflect the hierarchical structure of river drainage networks in large mainland basins and in smaller insular drainages (Cook et  al. 2007, Bentley et al. 2010). Recolonization of connected habitats following disturbances can sustain their populations and community structure. In coastal rivers and lakes, some marine-derived species have adapted to freshwater and can dominate freshwater communities. In these lowland rivers, there are important connections among deep pools and slack-water habitats that allow different species to disperse. For example, alterations of flow rates can alter long-term sustainability of atyid and palaemonid shrimps (Price and Humphries 2010). The persistence of many freshwater decapods depends on their migratory routes not being blocked by natural barriers such as waterfalls or massive landslides or by dams and poor water quality (Covich et al. 2009). Other species are found in headwaters of highly connected drainage networks and in associated wetlands along the margins of lakes and rivers. Many species have adapted to colonize and reproduce in temporal, vernal pools, seasonal wetlands, and other temporary habitats that are hydrologically complex (Colburn 2004). Migrations, Salinity, and Life History Patterns Palaemonid and atyid shrimps, as well as potamonid and gecarcinid crabs and crayfish, include species with distinct differences in salinity tolerances as they complete their life cycles (Ng 1988, Fievêt et al. 2001, Freire et al. 2003, Bauer and Delahoussaye 2008). Some studies indicate crayfish and crabs overlap in distributions, whereas other studies suggest that crabs use different habitats along



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elevational gradients (Álvarez et al. 20012, Lara et al. 2013). Most palaemonid shrimp species have an extended planktotrophic larval development, as do marine species (Rome et al. 2009, Ituarte et al. 2010). Several species of Macrobrachium, Palaemon, and Palaemonetes are in early phases of adapting to freshwater habitats. They generally have larvae that require high salinities to complete their development. Other species that are completely adapted to freshwater habitats have an abbreviated larval development with just a few, short-duration, nonfeeding larval stages and a smaller number of larger eggs (Odinetz-Collart and Magalhães 1994, Villalobos and Álvarez 1999, Mashiko and Shy 2008, Mejía-Ortíz and López-Mejía 2011). Species of Macrobrachium are mostly distributed in the tropics and subtropics (Bowles et al. 2000, Bauer 2004, De Grave et al. 2008, Chen et al. 2009, Wowor et al. 2009) and usually live in rivers that are connected with estuaries. Although most species’ life histories still require high salinities for the larvae to develop completely, M. amazonicum is one of the most widely distributed species and has adapted to live in estuaries as well as in completely inland freshwater habitats (Charmantier and Anger 2011, Pantaleão et al. 2011). Some species, such as M. acanthurus, live in estuaries but rarely move upstream. Many others, such as M. carcinus and M. faustinum, have postlarvae that migrate considerable distances upstream where they grow and reproduce. Their larvae are transported downstream during high-flow storm events back to saline waters, and the benthic postlarvae move upstream to complete the life cycle in freshwater (Bauer 2004, Covich et al. 2009). The avoidance of fish predators at lower elevations may be important drivers of these upstream migrations and complex life cycles. In addition, there may be adaptive value to disperse along any river to avoid intra- and interspecific competition. The concept of “ideal-free distribution” considers the behavior of individuals that move among two (or more) alternative habitats in search of the most easily accessible, highest quality habitats. The predicted end result is relatively similar densities across the array of locations because quality changes dynamically with incremental effects of increasing densities in each habitat (Fretwell 1972). There may be additional benefits in avoiding crowding beyond avoidance of competition that include lower risk of parasite and disease transmission. For example, postlarvae of M. ohione, M. potiuna, and M. rosenbergii become infected with different species of bopyrid isopods, Probopyrus pandalicola, P. floridensis, and P. buitendijki in their gill chambers (Masunari et al. 2000, Conner and Bauer 2010, Choong et al. 2011). The parasite feeds on hemolymph and weakens the hosts. It is likely that infection rates increase in crowded populations close to estuaries where copepods that serve as intermediate hosts are abundant. The trade-off for dispersing too far upstream is that females release their larvae to drift downstream where longer distances result in lower mortality. Alternatively, female M. ohione can apparently migrate long distances downstream to release their larvae that require higher salinities than found in the river waters (Bauer and Delahoussaye 2008, Rome et al. 2009). However, these females may be exposed to more fish predation. Many endemic species of freshwater crabs can complete their entire life cycle in freshwater habitats and have direct development, whereas others (such as grapsids) retain a life history characterized by well-developed free-swimming larvae (Ng 1988). Those species with “complete abbreviation” in the life cycle include females that produce a relatively small number of larger, yolk-rich eggs. These eggs are carried ventrally on the female’s pleopods, and the eggs hatch directly into small crabs rather than planktonic larvae. These young crabs are brooded by the female under her abdomen for several weeks. This same level of parental care is typical of most crayfish and demonstrates the importance of adapting to variable environmental conditions (Vogt and Tolley 2004, Vogt 2013). Some freshwater amphipods and atyid shrimps also have adaptations to increase survival of offspring (Tarutis et al. 2005, Huguet et al. 2011). In general, females carry their young and seek well-oxygenated, safe sites as part of their parental care. As mentioned previously, detailed studies of bromeliad-dwelling grapsid crabs (M. depressus) and other crabs in tree holes demonstrate the importance of parental investment in some species (Diesel 1997, Bayliss 2002). Similarly, the intensive maintenance of snail

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Freshwater Crustaceans shell middens as habitats for rearing Sesarma jarvisi is another example of highly developed adaptations for exploiting new nonmarine habitats (Diesel and Horst 1995). Some species develop cryptic coloration and minimize their movements as “sit-and-wait” predators. Protective behavior, such as carrying shells or camouflage while foraging, apparently has not evolved often among freshwater species. Although more than 1,000 species of hermit crabs use shells for protection in coastal marine habitats, only one species of freshwater crab (Clibanarius fonticola) is known to use abandoned snail shells to lower exposure to predators (McLaughlin and Murray 1990). This endemic species lives in a karstic spring-fed pool on Espiritu Santo Island in the Republic of Vanuatu, in the southwest Pacific. Its unique life history includes use of empty freshwater shells (Clithon corona) for protection. These karstic limestone pools are also the specialized habitat of the insular freshwater isopod Exosphaeroides quirosi. Similarly, the amphibious grapsid crab S.  jarvisi uses freshwater microhabitats in snail shells in Jamaica (Diesel and Horst 1995). Copepods are especially well adapted to live in tank bromeliads, pitcher plants, leaf axils, and tree holes (Reid 2001). Biofouling, Carapace Cleaning, and Ectoparasites Freshwater crustaceans are often effective in cleaning their gills and carapaces between molts (Bauer 1998). However, some decapod species are limited in keeping ectoparasites at low levels (Bauer 2002). Freshwater habitats have fewer encrusting species than marine habitats, yet certain species such as the temnocephalans (Platyhelminthes) and the branchiobdellids (Annelida) have evolved commensal and ectosymbiotic relationships with crayfishes. The branchiobdellids benefit their hosts under some conditions by cleaning material from host crayfish’s gill filaments (Brown et al. 2012). The costs and benefits among commensal species varies with the types and densities of the biofouling species and host capacity for cleaning (Lee et al. 2009). Other ectoparasites also occur among crayfishes; for example, the invasive P. clarkii hosts an invasive ostracod, Ankylocythere sinuosa (Aguilar-Alberola et  al. 2012)  and an invasive bivalve, Dreissena polymorpha (Gonçalves et al. 2013). Dreissena polymorpha (zebra mussel) settle on hard surfaces, including inorganic substrata and biological surfaces such as carapaces of crayfishes (Orconectes limosus, Orconectes rusticus) and a range of freshwater organisms (Ďuriş et al. 2007, Brazner and Jensen 2000, Gonçalves et al. 2013). Because adult crayfish molt at longer intervals than do juveniles, the number of filter-feeding zebra mussels accumulates on adult crayfish, and their foraging is likely diminished. Crayfish encrusted with mussels move more slowly and must spend more energy as a result of carrying this load of attached bivalves. It is unclear if these attached mussels increase or decrease risk of predation. Fishes that feed on zebra mussels would likely be able to consume the crayfish as well as the mussels. Crayfish derive energy from suspended particles by filter feeding (Budd et al. 1979) even though they also forage on a wide range of other foods that differ in size and type. Competition with zebra mussels for suspended organic material could have a negative effect on adult crayfish under some conditions. In general, freshwater crustaceans have evolved many ways to obtain energy, as well as to save some energy reserves for specific needs during stressful periods. Most importantly, many species feed on a wide variety of foods and can function effectively as detritivores (Crowl et al. 2001, 2006, Moulton et al. 2010, 2012, Duarte et al. 2012), herbivores, or omnivores (Parkyn et al. 2001, Usio and Townsend 2002). Stable isotope analyses have demonstrated distinct sources of foods (e.g., March and Pringle 2003, Mantel and Dudgeon 2004, Mantel et al. 2004, Rudnick and Resh 2005, Yam and Dudgeon 2005, Winemiller et al. 2011a,b, Burress et al. 2013). These analyses are especially useful for determining when decapods such as P. clarkii consume terrestrial plants foods in conjunction with drying of their habitats (e.g., Grey and Jackson 2012). Even when species feed on a wide range of foods, they apparently assimilate most of their energy from only a few of the available types of foods (Brito



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et al. 2006). In addition to some filter feeding, as noted previously, crayfish often use their mandibles to shred leaf litter and to consume many types of invertebrates (e.g., molluskan prey, Table 13.1).

FUTURE DIRECTIONS Studies of inland crustaceans will need to be placed in a broad regional and global context given the change in scale of climatic and human disturbances that is expected to affect inland waters, both freshwater and saline habitats (Williams 2002). Some species will likely increase in abundance and expand their geographic ranges, whereas others will be at greater risk of local and even global extinction (Strayer and Dudgeon 2010, Cullen et al. 2014). In the past, changes in species richness and in distributions of key indicator species were effective in monitoring water quality. As hydrological variability becomes less predictable and water diversions increase, there will be more complex relationships than previously observed. New studies will likely need to consider continual shifts in species relationships and how these species assemblages respond to the emerging physical and chemical conditions. The spread of disease vectors such as mosquitoes and snails is likely to increase as more landscape-level changes occur in inland habitats. These increases will require a more thorough study of the potential use of crustaceans for biological control. After decades of limited study, the use of natural biodiversity to limit vectors of diseases is being reconsidered in the search for sustainable solutions that limit resurgence of diseases once initial chemical controls have been partially successful. Documentation of new species in rich tropical waters will continue to help provide an array of different potential control strategies based on increased understanding of population dynamics, food web complexity, and dispersal capabilities of crustaceans. Although currently there still is a well-defined and remarkable diversity of freshwater crustaceans in extremely different types of inland habitats, many species remain undiscovered. Further studies are also urgently needed to understand how species interactions affect community composition and structure once invasive species become established. The impacts of invasive species, when coupled with other sources of disturbance, will increase rapidly and widely if guidelines for protection of vulnerable species cannot be established and enforced (e.g., Lodge et  al. 2012, Gallardo and Aldridge 2013). New biological communities are forming in response to these changes and, in particular, to shifts in distributions of non-native species. The value of many inland crustacean species that are small and often unseen is still unappreciated by those lacking information on the vital roles that crustaceans play in providing society with both clean water and food supplies. The “invisible” declines of groundwater and widespread lack of understanding of how surface and below-ground waters are connected creates many complex issues. Consequently, numerous species have already declined or disappeared as a result of water pollution and overexploitation of freshwater resources. Many unique species are highly specialized for living in a single location and are especially vulnerable. Other widespread species may not survive if their environmental conditions change abruptly because of a combination of natural- and human-generated disturbances. The capacities for sustainability of inland water are being severely tested, especially in regions where groundwaters are being pumped for different human uses faster than they can be recharged. In other regions, water diversion, surface or subsurface storage, and transfers are making the impacts of drought even more stressful to those species living in complexly interconnected habitats. Studies on potential impacts from climate changes and economic development on the dispersal and survival of endemic species are just beginning (e.g., Pipan et al. 2010, Shepherd et al. 2011, Murphy et al. 2013). Many opportunities are evident and highlighted by recent reviews (e.g., Balian et al. 2008, Covich 2009, Collins et al. 2011). Much of the previous research focused on high-latitude

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Freshwater Crustaceans locations where academic units and museums of natural history functioned as centers for training and research. These earlier baselines studies will be valuable to document changes. For example, future study will likely examine movements among species from warm tropical and subtropical to higher latitudes where extended species ranges are anticipated in response to warmer winters. Given a general need for fundamental understanding of ecology and evolution, opportunities are expanding in tropical and subtropical regions. As a consequence, many recent studies have documented high biodiversity along with new ecological relationships. A few topics are suggested here to illustrate connections among studies of evolutionary biology, biogeography, and animal behavior that may provide timely insights to resolve future problems. These examples illustrate the importance of documenting the global scale of changes in climate and land use that are creating fragmented habitats, longer droughts, and novel ecosystems. A common theme in this section is dispersal and movement among different habitats and variable patches of available resources. Central Place Foraging and Spatial Memory As discussed previously, some crustacean species move laterally among spatial refugia while seeking high-quality foods and minimizing their losses to predators, just as others move vertically within deep lakes to forage while avoiding predators. These lateral movements among crustaceans provide excellent opportunities for studies of foraging behavior to compare species under particular environmental conditions. Models of foraging theory (Stephens and Krebs 1986) typically postulate that the rate of immediate feeding is maximized by selecting prey items with sufficiently high profitability (energy per unit handling time). But when items must be transported to a refuge, this prey choice criterion can vary dynamically. The difference in timing of consumption at a refuge is a key component of the central place foraging model (e.g., Covich 1976, 1987). Handling time is less important when prey items are transported to a nearby central place for refuge because handling time is short relative to travel time (Fig. 13.5). Foraging among freshwater decapods may be most often limited by the travel-time costs for finding widely distributed foods (Gherardi et al. 1989). If these consumers eat “on the run” while searching for additional foods, then the distances traveled during foraging may be limited by the energy costs of finding foods and of defending feeding territories. Vigilance and increased energy expenditure in defending spatially distributed burrows used for refuge is expected to be adaptive among those decapod species living in habitats with highly variable water levels and pulsed supplies of food resources where there is also a high risk of exposure to predators. During wet periods, these decapods can move back and forth while carrying their larger or most “high-value” items (e.g., protein-rich foods such as thick-shelled snails that require a longer time to manipulate and consume when foraging) into their burrows or to other types of shelters (e.g., under rocks and root mats). Within the refuge, they can protect their food from being taken by competitors (Covich 1987). For example, in Neotropical streams, M. carcinus carries thick-shelled gastropods into burrows, and empty shells (middens) accumulate at the entrance (personal observation, A.P. Covich). Crabs (Epilobocera sinuatifrons) in Puerto Rican streams store seeds in burrows for various lengths of time, and this storage is adaptive during dry periods when foraging is restricted (personal observation, A.P. Covich). Food-storage behaviors are especially adaptive among relatively long-lived decapods, especially if there are short periods of localized food surplus followed by periods of food scarcity. Shared use of burrows over time is hypothesized for some species to allow for indirect, unintended sharing of protective cover, thermal refugia, and access to water during dry periods. This hypothesis regarding the benefits of central-place foraging around one or more burrows can be tested among foragers with well-defined and perhaps overlapping home ranges when water levels decline seasonally and distances traveled become limiting during



Alan P. Covich

Fig. 13.5. Central-place foraging from multiple burrows. The space (small open circles) around each burrow (small solid circles) indicates the “safe” foraging areas under average risk of predation. The concentric dashed circles indicate larger areas for foraging among individuals when predators are absent or during nighttime foraging among decapods. The distances traveled during foraging increase when predation risk is low.

foraging (Table 13.2, Fig. 13.5). For example, as water levels decrease, densities of both predators and prey species become concentrated in remaining pools, and predator–prey encounter rates increase (e.g., Covich et al. 2006, 2009). Some prey species, such as thin-shelled gastropods, are known to move into burrows to access water. Some of the snails crawling into burrows created and occupied by decapods are consumed, and the crayfish predators then can avoid foraging outside the burrow (personal observations, A.P. Covich). These types of seasonal interactions may be of particular interest for evaluating the effectiveness of various species of decapod predators in biological control programs. Burrowing Behavior Classifications of burrowing behaviors are available for characterizing those primary burrowing species that always construct burrows and the secondary burrowers that are more opportunistic. However, there is a need to learn about functional differences. Are the most effective shelters shared or aggressively defended for individual use? Are some burrow designs more effective than others to avoid desiccation? For example, is lack of dissolved oxygen a limiting factor for species that dig deeply to obtain water and/or to avoid high temperatures that lead to desiccation? Are burrows with multiple entrances more adaptive in avoiding predation and possibly overcrowding, as well as more likely to supply sufficient atmospheric oxygen for species able to use it? Those shelters with a single entrance and shallow depths may be adaptive in some locations or seasons but not in others. Some of these distinctions are well documented (e.g., Hamr and Richardson 1994, Noro and Buckup 2010). Additional comparative studies would be useful to define how these burrows function relative to foraging behavior and food storage (Growns and Richardson 1988). Additional types of microhabitats occur where one crustacean provides shelter for others that make most current classifications incomplete relative to ecological interactions. Some semiterrestrial species create their own microhabitats by burrowing deep into the sediment during dry periods. More studies are needed to further develop the concept of pholeteros, or faunal assemblages that occur in burrows (Lake 1977). For example, small species share burrows with larger species in Australian species when five coexist in dry regions (Fig. 13.6; Johnston and Robson 2009a, 2009b). Six species of copepods share crayfish burrows (Parastacus defossus) in southern Brazil, and the

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D A (1) (2)

B

C

Groundwater

(3)

Fig. 13.6. Commensal use of burrows by three crayfish species (A)  Gramastacus insolitus, (B)  Geocharax falcata, (C) Cherax destructor, and spatial relationships. (D) Examples of distributions include G. insolitus estivating in a crack (1) and a shallow depression (2) off to the side of a burrow constructed by G. falcata or C. destructor (3). Modified from Johnston and Robson (2009a), with permission from John Wiley and Sons.

copepods apparently rely on the crayfish-constructed burrows in the floodplain during cyclical dry periods (Reid et al. 2004). Isopods, amphipods, ostracods, and other small crustacean also are known to live in crayfish burrows (Williams 2006). Some species only use previously constructed burrows and are not known to create their own burrows. Yet, it is not clear why only certain species substitute constructing their own burrows by using whatever shelters already available (under large rocks and logs) unless the cost of construction is higher in some locations or seasons than others. New questions continue to emerge based on what is already known. For example, does energy invested in burrow construction increase the value to an individual? Does this investment require additional energy needed to defend its use? Does the value of a shelter and its defense costs increase if its location is in an area where food resource availability is relatively high? Research is beginning to study movement and use of space



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by decapods to determine absolute and relative values that individuals have for specific resources. For example, past ownership of a burrow is thought to increase the value of a site. This higher valued location may increase the aggressive behavior among some crayfish (Austropotamobius pallipes) in defending use of their burrow (Tricarico and Gherardi 2010). A related area of study relates to how long species can identify a location and how that memory can influence their use of space. Studies demonstrate that some decapod species appear to have well-developed spatial memory (Vannini and Cannicci 1995, Gherardi et al. 1998a,b) and will return to home burrows. This site fidelity occurs even if sometimes these locations are occupied by other individuals (Fero and Moore 1998). However, several studies in rivers and canals report no strong support for spatial memory beyond short nocturnal trips from burrows or other refuges for seeking mates or foraging up- or downstream (Robinson et al. 2000, Bubb et al. 2008).

CONCLUSIONS After millions of years of evolutionary adaptation on a global basis, the high diversity of crustaceans in inland waters on every continent is not surprising. The summary of some of these known widespread species successes is used here to illustrate their tolerances to environmental conditions in many extreme habitats ranging from very saline to dilute and from hot to cold waters. However, this review of adaptive mechanisms for dispersal and tolerance of extreme conditions should not suggest that most or any of these species will be able adjust to the expected increases in extreme variability that can result from rapid climatic changes. Many crustacean species are widely distributed in shallow and temporary as well as in deep and permanent waters. Isolated springs and caves are important habitats for endemic species that are vulnerable to increased pollution and groundwater diversions. The highest species diversity is found in ancient lakes and rivers where evolution has resulted in complex communities and food webs. The value of crustacean diversity is evident in the many ways that particular species provide essential shellfish production used by people all over the planet. These values for food production are readily quantified, whereas the importance of crustaceans as sources for biofiltration and breakdown of organic matter are less often evaluated but remain essential for sustaining clear water. The various roles of decapods, copepods, and ostracods for biological control are other examples of the importance to society for sustaining biological diversity among crustaceans in a wide range of habitats.

REFERENCES Abele, L.G., and W. Kim. 1989. The decapod crustaceans in the Panama Canal. Smithsonian Contributions to Zoology 482:1–50. Acquistapace, P., L. Calamai, B.A. Hazlett, and F. Gherardi. 2005. Source of alarm substances in crayfish and their preliminary chemical characterization. Canadian Journal of Zoology 83:1624–1630. Affonso, I.D., and L. Signorelli. 2011. Predation on frogs by the introduced crab Dilocarcinus pagei Stimpson, 1861 (Decapoda, Trichodactylidae) on a Neotropical floodplain. Crustaceana 84:1653–1657. Aguilar-Alberola, J.A., F. Mesquita-Joanes, S. Lopez, A. Mestre, J.C. Casanova, J. Rueda, and A. Ribas. 2012. An invaded invader: high prevalence of entocytherid ostracods on the red swamp crayfish Procambarus clarkii (Girard, 1852) in the eastern Iberian Peninsula. Hydrobiologia 688:63–73. Alexander, J.E., and A.P. Covich. 1991. Predator avoidance in the freshwater snail Physella virgata to the crayfish Procambarus simulans. Oecologia 87:435–442. Álvarez, F., J.L. Villalobos, G. Armendáriz, and C. Hernandez. 2012. Biogeographic relationship of freshwater crabs and crayfish along the Mexican transition zone: reevaluating Rodríguez (1985) hypothesis. Revista Mexicana de Biodiversidad 83:dx.org/10.7550/rmb.28230.

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14 CRUSTACEANS OF EXTREME ENVIRONMENTS

Chiara Benvenuto, Brenton Knott, and Stephen C. Weeks

This chapter is dedicated to Brenton, a dear friend and outstanding colleague, who dedicated much of his life to the study of crustaceans. Brenton, your legacy will continue.

Abstract Crustaceans are a remarkably diverse group of organisms that have colonized and occupied a broad variety of niches. Many crustacean species are found in extreme environments, inhospitable to the majority of animal taxa, including Antarctic lakes, subterranean waters, hydrothermal vents, dry deserts, hypersaline lakes, and highly acidic habitats. Particular adaptations have evolved in response to the environmental conditions in these extreme habitats, shaping the lifestyle of crustaceans. In this chapter, some of the morphological, physiological, and life history adaptations that enabled crustaceans to colonize these habitats are reviewed. An overview of the main crustacean taxa in these extreme environments is given, and their evolutionary adaptations are briefly compared to those of other organisms co-occurring in the same habitats. Although not exhaustive, this review highlights how successful crustaceans have been in adapting to extreme conditions. Nowadays, anthropogenic activities risk irreversibly altering the delicate equilibrium these crustaceans have achieved in extreme environments.

INTRODUCTION Crustaceans, a very speciose group of organisms surpassed only by insects, mollusks, and chelicerates, present an impressive array of morphological diversity, the highest among metazoans (Martin and Davis 2001). Their variety in morphological traits, combined with physiological, ecological,

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Crustaceans of Extreme Environments and behavioral differences, underscores a high level of adaptation to a wide range of environments and conditions (Thiel and Duffy 2007). Crustaceans have colonized and filled almost every type of niche available, including the most inhospitable places on our planet, such as Antarctic lakes, subterranean waters, hydrothermal vents, xeric deserts, hypersaline lakes, and highly acidic habitats. These environments are hostile to the majority of other multicellular organisms, yet selected crustaceans thrive within them. Ecosystems are regulated by complex interactions among organisms. The ecological dynamics connecting these organisms are arguably the most important factors shaping species’ distributions. In extreme environments, the ecosystem is usually much simpler, and abiotic factors play a major role in determining species’ presence and abundance (e.g., Convey 1997), even though biotic factors are still important (Camacho 2006). Abiotic factors include physical (e.g., temperature, pressure, light) and chemical (e.g., salinity, pH, dissolved oxygen) parameters. Extreme environments constitute an array of abiotic factors beyond the extremes of the limits of tolerance of the majority of organisms. Extremophiles “love” these extreme conditions, or at least can resist and persist in them (Rothschild and Mancinelli 2001). The sense of wonder for these creatures contributed to the creation of names that highlight their ability to survive in extreme conditions:  thermophiles, psychrophiles, acidophiles, alkaliphiles, halophiles, xerophiles, and piezophiles resist extreme high temperature, coldness, acidity, alkalinity, salinity, desiccation, and pressure, respectively. Furthermore, many organisms are indeed poly-extremophiles, enduring in environments where more than one parameter is “extreme” (Rothschild and Mancinelli 2001). Depending on the ability to sustain narrow or large variations in abiotic parameters, organisms are classified as “steno” or “eury,” respectively. Steno-organisms can survive only within limited variations of the parameters to which they are adapted. We might regard them as the best examples of extremophiles because they are perfectly adapted to specific extreme conditions (low or high temperatures, low or high salinity, etc.). Alternatively, extreme environments may present considerable variation in one or more parameters that can be tolerated by eury-organisms (Peck 2004). When environmental conditions fluctuate greatly over time (e.g., in temporary environments, such as ephemeral pools filled by rain only for a short season or Antarctic lakes that freeze solid in winter), specific stress-avoidance strategies can be used by organisms (Badyaev 2005), including migration, production of desiccation-resistant cysts to survive the lack of water, hibernation, or supercooling to persist in cold conditions. Some crustacean species are adapted to extreme environments and share their habitats with many microorganisms and a few other multicellular organisms. Because of specialized biological adaptations, many species are endemic to their extreme habitats (Rogers et  al. 2007). Here, we summarize the characteristics of extreme environments and present an overview of some of the morphological, physiological, and life history adaptations that enabled crustaceans to colonize these habitats. These evolutionary adaptations are briefly compared to those of other organisms cohabiting the same environments (Tables 14.1 and 14.2).

CRUSTACEANS IN ANTARCTIC LAKES Antarctica is the most extreme of all continents. Large and isolated, it is the coldest and windiest continent of our planet, characterized by extremely dry weather and almost completely covered by snow and ice during most of the year (Convey 1997, Peck et al. 2006). A biological designation of the Antarctic includes not only continental and maritime areas but also subantarctic islands. Antarctic lakes display considerable diversity in terms of size, depth, salinity, temperature, age, and seasonality: some freeze solid or dry out completely (temporary lakes), others are permanently

Table 14.1.  Extreme environments: organisms other than crustaceans Conditions/ Characteristics

Taxa Present

Adaptations

Acarina1

(littoral species)

Anellida: Oligochaeta

Antarctic Lakes

2–4

Low temperature Poor light climate Nutrient limitation Salinity

Bacteria/Cyanobacteria5, 6

Biochemical adaptations

Diptera: Chironomidae3, 4

Flexible life cycle; overwintering as larvae and/or adults

Gastrotricha2 Nematoda2, 9, 10

Euryhaline species in saline lakes; anhydrobiosis and cryobiosis

Phytoplankton/ Diatoms5, 6, 11

Mixotrophy; starch reserves; cysts; nutritional versatility; high mobility

↓ Truncated food webs Species poor biota

Platyhelminthes2 Protozoa5

Mixotrophy

Rotifera

2, 6, 12

Tardigrada2, 12

Anhydrobiosis and cryobiosis

Amphibia13, 14 Arachnida13, 15

Pigment reduction in the eyes or lack of eyes

Chilopoda13 Subterranean Environments

Coleoptera13, 16 Scarce food Anoxia Aphotic environment ↓ Truncated food web

Lack/reduction of eyes; pigment reduction; wing reduction

Diplopoda13 Fish13, 17, 18

Eye reduction; pigment reduction

Insecta [Collembola; Diplura; Diptera]13 Molluska13, 19, 20

Eye loss; shell size reduction; lack of tegument pigmentation

Oligochaeta13, 20 Protozoa20 Turbellaria13 (Continued)

Table 14.1 (Continued) Conditions/ Characteristics

Taxa Present

Hydrothermal Vents

Annelida/Tubeworm21–23

High temperatures High hydrostatic pressure Anoxia Presence of hydrogen sulfide and heavy metals Aphotic environment

Adaptations Symbiotic chemolithoautotrophic bacteria; use of carbonic anhydrase to concentrate carbon; protection by a chitinous tube; phenotypic plasticity; use of myohemerythrin instead of hemoglobin; escape responses

Chemosynthetic bacteria24

Gasteropoda/Bivalves22 Acarina25

Symbiotic methanotrophic and sulfur oxidizing bacteria (aquatic mites)

Amphibia25–27 Diptera: Chironomidae25–27 Desert Environments Temporary Freshwater Pools

Fish28, 29 Heteroptera27 Extreme hydrological regimes

Insecta [Coleoptera27/ Notonectidae/ Corixidae/Culicidae/ Ceratopogonidae]25, 26 Molluska25 Nematoda25 Odonata26, 27, 30 Rotifera25 Tardigrada25

Desert Rivers

Turbellaria30 Acarina31 Extreme hydrological regimes

Annelida31 Insecta: Coleoptera/ Diptera31 Molluska31

Fossorial habit; cutaneous respiration

Table 14.1 (Continued) Conditions/ Characteristics

Taxa Present

Adaptations

Desert Spring

Insecta: Coleoptera/ Diptera/ Ephemeroptera/ Hemiptera/ Lepidoptera/Odonata/ Trichoptera32 Molluska32

Desert Saltwater Ponds/ Lakes

Turbellaria32 Extreme hydrological regimes Salinity ↓ Species poor biota

Acarina33 Coleoptera33, 34 Diptera33 Fish34 Hemiptera34, 35 Molluska: Gastropoda33 Nematoda35 Odonata35 Amphibia36, 37

Reduced sodium content in the body

Bacteria38

Chemolithoautotrophic; sulfur-oxidizing; resistant spores

Acidic Environments

[Coleoptera39, Megaloptera]40 pH 1 year in the case of the amphipods Niphargus virei and N. rhenorhodanensis), reducing their metabolic, locomotory, and ventilatory rates in the process (Hervant et al. 1999). Hervant and Renault (2002), studying aquatic isopods, suggest that during long-term starvation, stygal crustaceans rely on large energy stores, subsisting mainly on lipids and sparing proteins and glycogen; surface crustaceans going into fasting show an immediate decrease in all energy stores. Cave waters typically show low oxygen concentrations, and stygobiontic amphipods and isopods survive severe hypoxic conditions far longer than do epigean forms (Hervant and Mathieu 1995). Crustacean stygobionts show a characteristic morphofacies or troglomorphy: lacking pigment, eyeless, and having elongate limbs and sensory structures (Fig. 14.1). Because there is no debate

Fig. 14.1. Troglomorphy exemplified in the subterranean amphipods Niphargus aquilex (left) and N. fontanus (right). Photo courtesy of Dr. Joerg Arnscheidt.

395

396

Crustaceans of Extreme Environments about the ultimate source of stygobionts—namely, from surface populations—the lack of both pigment and eyes exemplifies regressive evolution. There has been, however, considerable debate concerning the mechanism(s) leading to these losses. What are the selective advantages of lacking pigment, of being eyeless in a subterranean environment? Arguments in support of selection invoke energy economy (in an energy-depleted environment, the limited reserves available are better expended on producing adaptive structures and reproduction rather than on producing nonadaptive structures) and pleiotropy (the regression may be due to negative pleiotropy linked with, for example, elongation of antennae that may be selected for in completely dark environments or exemplify positive pleiotropy associated with structures selected against in caves). Alternatively, structures with no adaptive benefit may be lost by the accumulation of neutral mutations and genetic drift (Poulson 1964, Culver 1982, Howarth 1987). Deleterious mutations for pigment and eye development may accumulate because they would have no effect on fitness of cavernicoles and would not be eliminated by selection; thus, these characters may be lost by drift in the absence of selection. Studies on natural systems have not generated a consistent model explaining the regressive morphological features of cavernicoles. In one detailed study into the adaptation of the amphipod Gammarus minus to the groundwaters of the eastern United States (where the morphofacies range from troglomorphic populations in two cave areas in Virginia to amphipods from springs with no troglomorphic expression), Culver et al. (1995) assessed five criteria proposed by Brandon (1990) by which adaptation might be accepted as an explanation for how cavernicoles have evolved. The five criteria include (i) evidence of selection, (ii) an ecological accounting for differential rates of reproduction, (iii) evidence that the cave morphofacies have heritable components, (iv) data concerning gene flow and genetic relatedness of surface and subterranean populations, and (v) information on ancestral and derived character states. Culver et al. (1995) concluded that eye size of this amphipod changes through selection and neutral mutations, but antennae and body size change through selection only. Enlargement of nonvisual sensory structures is widely interpreted to exemplify a selective advantage, but supporting evidence is meager. Holsinger and Culver (1970), comparing cave and spring populations of G. minus in Virginia, argued, on the evidence of significantly different slopes plotting average body length of males from seven cave and eight spring populations, that there was an increase in length of antennae 1—but the genetic basis was unknown. Although subterranean communities often are simpler than epigean communities in terms of species number, interactions nonetheless occur. In Appalachian caves, amphipods and isopods concentrate in riffle zones of cave streams away from predators and in the zone where the oxygen content is increased and leaves accumulate. Interactions between the two crustaceans in the riffles may involve competition for food, with small or damaged specimens being cannibalized/eaten by larger specimens or being swept from protective spaces into the water column and into pools harboring predators (Culver 1975). However, the valviferan isopods Caecidotea cannulas and C. holsingeri co-occur in Alpena Cave, Virginia, without any evidence of competition between the species (Culver 1994). The two may coexist sans competition because their size difference (C. annulas is larger than C. holsingeri) enables them to exploit differences in sizes of rocks and gravel. Habitat partitioning is implemented also to manage intra- and interspecific interactions (Luštrik et al. 2011): small individuals of the surface amphipod Gammarus fossarum and the subterranean amphipod Niphargus timavi inhabit finer substrata, less used by adults of these two coexisting species (to avoid predation/cannibalism as well as competition). Stygobionts, and especially the crustacean representatives, are important because of the insights they provide into past geographical connections. The freshwater stygobiontic crustaceans from the Pilbara region of northern Western Australia (Amphipoda, Thermosbaenacea, Remipedia) through to related forms from the Caribbean constitute significant evidence of a Tethyan connection, now disjunct through continental drift (Humphreys 1993, Knott 1993).



Chiara Benvenuto, Brenton Knott, and Stephen C. Weeks

In view of this discussion of evidence of the success at which crustaceans colonized the underworld, it may not be cynical to suggest that the greatest problem confronting living underground stems not from the obvious biological issues of lack of light (restricting primary productivity) and lack of diurnal and seasonal cues to control life cycle activities, for example, but rather the human-driven, seemingly cosmopolitan trend to deplete aquifers of their water. The ecological and physiological problems have been solved, during the time available for the evolution of a wide diversity of stygobionts. In marked contrast, the depletion of aquifers through anthropogenic activities is immediate, leaving many stygobionts with no time to “find solutions” other than to be driven extinct.

CRUSTACEANS IN HYDROTHERMAL VENTS Dwellers of the abyss cope with considerable pressure—and they share two constraints with subterranean faunae: the lack of light precluding photosynthetically driven primary productivity and lack of reliable food supplies. Light of blue wavelengths penetrates much deeper into the water column than those of other wavelengths, with the depth depending on a number of factors including the angle of refraction and the clarity of the water column; photosynthesis (PS) is possible in the upper 100–200 m, but the depth to 1,000 m is dimly lit and thus not sufficient for PS. The depth across 90% of the area of the world’s oceans exceeds 1,000 m, and the water column at these depths lacks light (is aphotic). As with probably all habitable places, continuing study has identified heterogeneity of biotopes where originally it was thought homogeneity prevailed. For example, the great abyssal plains are not uniformly flat and covered with a uniform blanket of sediment. Instead the flatness may be interrupted in places by sea mounts (mountains derived from extinct volcanoes rising generally 1,000 m above the abyssal plain but not reaching sea level; 30,000 are estimated to occur) and the 55,000 km of ridges separating the continental plates that are the sources of spreading of tectonic plates. As recently as 1977, very localized hydrothermal vent chimneys (known as “black smokers”) were discovered at the comparatively shallow depth of 2,500 m on the East Pacific Rise (Corliss et al. 1979). Since then, numerous other hydrothermal vents have been recorded from the mid-ocean ridges of the globe, both fast spreading (≥12  cm/yr−1) and slow spreading (