SHELTER USE BY CALCINUS VEWLI, BERMUDA'S

EX?)ELflC HELMIT CL4B

Lisa Jacqueline Rodrigues

A thesis submitted in conformity with the requirements for the degree of Master of Science Graduate Department of Zoology University of Toronto

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The author retains ownership of the L'auteur conserve la propriété du copyright in this thesis. Neither the droit d'auteur qui protège cette thèse. thesis nor substantial extracts bom it Ni la thèse ni des extraits substantiels may be printed or otherwise de celle-ci ne doivent être imprimés reproduced without the author's ou autrement reproduits sans son permission. autorisation. Shelter use by Calcinus vemlli, Bermuda's endemic hennit crab.

Master of Science, 2000

Lisa Jacqueline Rodngues

Department of Zoology

University of Toronto

Calcinus vemlli, a hennit crab endemic to Bermuda, is unusual in that it inbabits both gastropod shells (Centhium Iitteratum) and gastropod tubes (Dendropoma irremlare and Dendropoma annulatus; Vermicularia knomi and Vermicularia spirata). Field surveys found significantly more maies inhabiting shells and significantly more females inhabiting tubes. In the laboratory no significant difference was show in shelter choice for males or females. In a second choice experiment, males showed no discrimination between gastropod extract types, and females showed discrimination that related to the shelter they were collected in. In a cornpetition between the sexes, the winner of the intact shell was found to depend upon relative shield length and relative major chela length. Overall, males were found to be better exploitative cornpetitors than fernales. A significant difference in uropod asymmetry was found; tube dwellers were more syrnmetrical than shell dwellers. A shelter manipulation experiment found shelter type to be important in determining asymmetry. The distribution of c. vemlli between shells and tubes may be an example of "making the best of a bad situation," if Polydora sp. is detrimental to the reproductive success of the hennît crab. Although there is jus my name attached to this thesis, there have been many people who have contributed and helped in the past two years.

First and foremost, thanks go to both of my supervisors, Dr. David Dunham and

Dr. Kathryn Coates. Wztlier I was in Semuda or Toronto, bcth had open doon or were available for on-line discussions. They supplied me with inspiration, as well as advice, and their questions always kept me on my toes.

Much of the field work and expenments that 1 conducted during the summer of

1999 could not have been accomplished without Matthew Hammond. As a Bermuda

Program student at BBSR Matt helped me with al1 aspects of the project, from collecting

and shucking hennit crabs to "sacrificing" gastropods.

My work involved transporting animals between Bermuda and Toronto. This was made possible by the issuing of nurnerous irnpon and export permits thanks to Brian

Luckhurst and Norbert Simmons of the Department of Fisheries, Coney Island, Bermuda and Mike Souza of BBSR. Mike Souza also measured and cut the Plexiglas pieces for the Y-mare apparatus, and constmaed some glas aquaria. I am also grateful to al1 of the staff of BBSR.

Patricia Pocklington introduced me to the wonderful world of polychaetes. She identified the polydorid that 1 found inhabiting the Cerithium litteraîum shells with

Calcinus vemlli.

Thanks to Dr. Robbie Smith for the use of the research boats, Mako and &a

Dance, to Nancy Stevens for the use of Mussel Pie. The boats were captained on most occasions by my dive buddies Sarnantha dePutron and Graham Webster, who were arnazingly able to find just the reef we wanted without the GPS. 1 am especially grateful to Sam for allowing me to search her sites for C. vemlli. Other dive buddies that made

SCUBA diving possible were Anne Savage, HaleIy Outerbridge, Eli Woolery, Alex

Chequer, and Dr. Joanna Pin. Quincy Burgess, Kevin ?, and Dr. Roger Pocklington had the job of'boat watcher' on nünerous occasions, which involved basking in the Bermuda sun for endless hours on a swaying boat to eventuaily drag aboard exhausted divers and their heavy buckets.

In the early months of this Master's program, 1 received incredible support from many people at the Bermuda Aquarium Museum and Zoo (BAMZ). Dr. Annie Glasspool,

Billy Mitchell, and Chris Flook helped me collect everything from snapping shrimp to decorator crabs. It was finally Dr. Wolfgang Sterrer who suggested that 1 take a look at C. verrilli; he thought they may result in something interesting, and he was right. 1 received moral support and well wishes from al1 of the stafFat BAMZ.

In Toronto, 1 was fortunate to work with two outstanding scientias, Nasreen

Rahman and Jan Richards. Erika Crosse helped me make slides and photographie prints of the hermit crabs. The hermit crabs were looked after by several work-audy students:

Michelle Herzog, Jennifer Tran, David Punzalan, Mary Sunderland, and Lesia Murray.

My roornmates, Deirdre, Denise, and Kathryn patientiy listened to al1 of my hermit crab tales. Finally, 1 thank my parents and brother for their love and support.

They have helped me in more ways than 1 can possibly list. This project was funded by a Bermuda Governrnent Scholarship, the Munson

Foundation through BBSR, Graduate htern Program of BBSR and a Natural Sciences and Engineering Research Council of Canada research grant to D. Dunham

Two CO-authoredscientific papers have been denved f?om some of the material in this thesis:

Rodrigues LJ, DW Dunham, and KA Coates (2000) Shelter preferences in the endemic

Bermudian hermit crab Calcinus verrilli (Rathbun, 190 1). Cmstaceana 73 : 737-

750.

Rodrigues U,DW Dunham, and KA Coates (Submitted) Gastropod shells or gastropod

tubes? Shelter choice in the hermit crab Calcinus vemlli. Modem A~oroachesto

the Study of Crustacea.

The first is paper based on Chapters 1 and 2 of the thesis; the second is based on Chapter

2.

1 designed and conducted ail of the field work and experiments, analyzed the data, did the appropriate library research, and wrote the research papers. Guidance and advice were provided during dl stages by Dr. D.W. Dunham and Dr. K.A. Coates. Title Page -- I

Abstract ii ... Acknowledgements - -.-- .-.-.-- ..+-- 111 .. List of Publications --.- -.------.-

Table of Contents vi

List of Tables - ix

List of Figures .-...-.--. xi

General Introduction

Hennit Crabs: Unique Members of the Subphylum Cmstacea --.....- -.-- 1

Shell Occupancy: Pros and Cons ....- 5

ShelIs: A Lirniting Resource - 7

Corn petition and S hell Exchange ------.-.------.------8

Alternative SheIters -- ..-..-...-....--.-- 9

Bermuda's Endemic Hermit Crab ..., ...----.-.-.----.-.- 14

Chapter 1

The distribution of Calcinus vemlli in Bermuda 17

Introduction 17

Methods 21

Updated Distribution - 22

Discussion -29 10. Chapter 2

Shelter preferences in the endemic Bermudian hennit crab, Calcinus verrilli-+--- 3 1

Introduction 3 1

Methods. ------34

Intraspecific competition in the endemic Bermudian hermit crab, Calcinus verrilli 61

Resu lts _...... _ ..-....._...-.--.-... 67

75 Discussion .___....-.-..-~-_---.-....-...-.--.- ...... ,......

12. Chapter 4

The effects of shelter type on uropod symmetry in Calcinus vemlii 78

Introduction --..78

Met hods. .-- 8 1

13. General Discussion

Field Surveys --- 96

Preference for Shelters . 97

Cornpetition for Shelters 99

A Polydorid Anecting Shelter Use 100 Morphological Differences 102

14. Appendix A

Regression analyses for gastropod shell measurements and Calcinus vertilli shield length 103

15. Appendix B

A new Poivdora sp. (Spionidaz, Polychaeta) found inside the gastrepcd shells of Calcinus O6 vemlli --- -.-. 1

16. References --.______I______I____c____._r____..____.._-_____I______I____c____._r____..____..______I______I____c____._r____..____.._...... _____I______I____c____._r____..____.._...... _____I______I____c____._r____..____..______I______I____c____._r____..____..______I______I____c____._r____..____.._..._____I______I____c____._r____..____..______I______I____c____._r____..____.._..,.-...-.- 108

viii LIST OF TABLES

1. Hennit crab species known to inhabit shelters alternative to spiraled gastropod shells

and the authors who first observed the association Il

2. Sites visited fiom May to September, 1999, and Apd to May, 2000, and the habitats

and shelter types occupied by Calcinus vemlli --.-. 24

3. The statisticai significance ofshieid length diffirsnces Semeen Calcinus rerrilli males

and females and shelter types, using (a) Mann-Whitney rank sum test and (b) Student's t- test ..-.-- 43

4. The number of males and fernale Calcinus vedli in the three types of shelters

coilected in the field - 45

5. Correlation coefficients obtained from linear regressions of Calcinus verrilli shield

length for each shell or tube measurernent ....-.- ...... --.- ...- +..---...... 48

6. The choices made in the Shelter Choice Experiment between the gastropod shell,

Cerithium 1itteratum, and gastropod tubes, Vermicularia spp, b y Calcinus vedli males

and females collected in different sheiters - - 52

7. The choices made in the Chemical Choice Expenment between the gastropod shell,

Cerithium litteratum, and gastropod tubes, Vernicularia spp, extract presentation arms

made by Calcinus vemlli males and females collected in different shelters 54

8. The results of shell competitions (a) between male and female Calcinus vemlli of the

same shield length and @) between C. vemlli females that were 10% larger than males,

at 2 hours and 24 hours after the introduction of a "good" shell. - 71

9. The results of shell competitions between males and female Calcinus vemlli when

males have a larger major chela than females (M>F), females have a larger major chela than males FM), and males and females have equal major chela lengths (M=F) at (a) 2 hours and (b) 24 hours der the introduction of a "good" shell------72

10. The results of shell competition between male and female Calcinus verdi when females were ovigerous (Ovig)or non-ovigerous (Non) at (a) 2 hours and (b) 24 hours after the introduction of a "good" shell . --- 74

11. The mean ieft (TI) and nght (X) uropod irngths (mm)of Calcinus veriilli forced tube- dwellers, forced shell-dwellen-V, and forced shell-dwellers-D over consecutive molts ------. --..+.---- 88

12. Cornparison of the final asymmetry indices (AI'S) for Calcinus verrilli forced dwellers at the end of the laboratory experiment with the Al's of the respective shelter dwellers in the field. Calculated with (a) Student's t-test and (b) Mann-Whitney rank sum test----...... --- A-....-...... -.....-.1....-...--..-+...+-...-...-..... -..--.....---. 92 LIST OF FTGURES

1. An extemal morphological comparison between (a) a typical malacostracan (lateral view) and (b) a herrnit crab (dorsal view). 2

2. A hermit crab (shaded) inside a dextrally coiled, transparent shell, showing the coiling of the abdomen and uropods around the columella of the shell -.-- 4

3. A map of Bermuda with the locations where Calcinus vemI1i was found prior to and

during the present study ------Pm-- ..-.--..-..P.. 18

4. A cross-section illustration of a "boiler" reef . -...---..- . 28

S. A drawing of a shell showing the dimensions that were measured for the regession analyses .....-.-.- 36

6. A drawing of the Y-maze apparatus using in the Chemical Choice Experiment 39

7. Calcinus vemlli shield length (mm) of males and fernales in three different shelter types in the field -44

8. The distribution of Calcinus vemlli males and females among three different shelter types in the field --- .,.-., 46

9. The relationship between hermit crab (Calcinus vemlli) size (shield length, SL) and shell (Cerithium litteratum) length inhabited by (a) males and (b) females in the field 49

10. The relationship between hermit crab (Calcinus verrilli) size (shield length, SL) and

Vermicularia spp tube opening diameter inhabited by (a) males and (b) females in the field 50 II. The relationship between hermit crab (Calcinus vemlli) size (shield length, SL) and

Dendro~omaspp tube opening diameter inhabited by (a) males and @) females in the field --51

12. A drawing of the major chela of Calcinus vedli, with arrow showing where measurements were taken 65

13. Linear regressions of Calcinus vemlli shield length (mm) against major chelr length

(mm) for males (solid line, filled points) and fernales (dashed line, clear points)- 69

14. Drawings of the lower abdomen of Calcinus vemlli From (a) a shell and (b) a tube --.. ~~~..+~~-.--...-.-..83

15. Box plots cornparhg the asymmetry indices of shell and tube dwellers of Calcinus

86 vedii in the field .-.--..----~..-.---....~~...--.....-.-...... ---. *.-...... -.---...--...-.... " ..-..--

16. Box plots of the asymmetry indices for Calcinus vemlli that were (a) forced tube- dwellers, (b) forced shell-dwellers-V and (c) forced shell-dwellers-D over several molts ------...------.- 89

17. The relationship between hermit crab (Calcinus vemlli) size (shield length, SL) and shell (Cerithium litteratum) width inhabited by (a) males and (b) females in the field 103

18. The relationship between hermit crab (Calcinus vemlli) size (shield length, SL) and shell (Cerithium litteratum) aperture length inhabited by (a) males and (b) females in the field - 104

19. The relationship between hermit crab (Calcinus vemlli) size (shield length, SL) and shell (Cerithium litteratum) aperture width inhabited by (a) males and (b) females in the fieid 105 GENERAI, INTRODUCTION

Hermit Crabs: Unique Members of the Subphylum Cmstacea

Hermit crabs are classified in the subphylum Crustacea, class Malacostraca, subclass Eumalacostraca, superorder Eucarida, order Decapoda, suborder Pleocyemata, infiaorder homura, and superfamily Payroidea (Forest, et d.,2000). Hennit crabs do not possess a hardened exoskeleton on their entire body. Only the cephalothoraic region of the body, which is covered dorsaily by the carapace, and bears the chelipeds (ln pair of walking legs modified for grasping) and pereiopods (2ndto 5h pairs of walking legs), is hardened following an adult molt. The abdomen of the crab remains soft and fragile. In place of the protective cuticle, hermit crabs usually cover their abdomen with natural, hollow objects, in particular gastropod shells. The shells can be carried around and perrnanently protect the abdomen. Ideally the animal should be able to escape from danger by withdrawing entûely into the shell. In some species, on withdrawal into the shell, the shell aperture is blocked by the major chela (Reddy and Biseswar, 1993).

Gastropod shells come in an array of different shapes (Abbott, 1954; Sterrer,

1986) and different hermit crab species show preferences for different shell variables.

Shell volume (Bertness, 1%O), colour (Partridge, 1MO), weight (Reese, I963), and species (Elwood, et al., 1979) have been shown to be related to preferences.

Alterations made to the malacostracan (Figure 1) have allowed hermit crabs to utilize gastropod shells. The abdomen of a diogenid is asymmetrically coiled, either dextrally or sinistnilly, to fit inside the shell and coi1 around the columnella (Figure 2).

There has been a reduction in the size and structure of the 4& and 5' pairs of Figure 1. An extemai rnorphological cornparison between (a) a generalized malacostracan (lateral view) and (b) a hennit crab (dorsal view). The labeled parts are the same in both diagrams: R, rostnim; CA, carapace; T, telson; U, uropods; PL, pleopods, with eggs shown on the hermit crab; PE, pereiopods (2ad -5 th walking legs); CH, cheliped (ld waiking leg); M, maxillae and maxillipeds (mouthparts), hidden behind the

2"d antennae in tne hermit crab; iA, i" antennae; X, ydanteniae; S, shield of the hermit crab. Figure la adapted from Remane, et al. (1989). Figure Ib adapted fiom Nybakken

(1996).

Uropod

Figure 2. A hennit crab (shaded) inside a dextrally coiled, transparent shell, showing the coiling of the abdomen and uropods around the columelfa of the shell. Adapted &om

Bliss (1982). pereiopods, the telson, and uropods, which allow the hennit crab to hold ont0 its shell. In

some cases, modifications to morphology are specific to the gastropod species utilized

(Selbie, 192 1; McLaughlin and BaiIey-Brock, 1975).

SheIl Occupancy: Pros and Cons

Shells are particularlç important because of the protection they provide against abiotic stressors, including physical abrasion and concussion, desiccation (Reese, 1969),

changes in salinity (Shumway, 1W8), temperature, and pH (Bertness, 198 1a, b), and against predators (Reese, 1969; Vance, 1972a). Therefore, they allow for tolerance to a broad range of environments. For fernales, protection is provided for her eggs, which are

attached to the pleopods and maintained inside the shell, for even as long as 3 months in

some species (Pike and Williamson, 1959).

Despite the benefits, shell occupancy has several costs associated with it. There is

an energetic cost of canying around a sheil (Herreid and Full, 1986). This cost may not

seem to be as high in water as it would be on land (i.e. for land hennit crabs,

Coenobitidae) due to the greater buoyancy of water. Ultimately, however, the cost of

carrying a shell in water is just as high as carrying one on land because of the greater

friction of a shell in water than in air (Elwood and Neil, 1992).

Shell species have also been shown to affect the mating success of males (Hazlett

and Baron, 1989). Calcinus tibicen males in Leucozonia spp shells were successfil at

obtaining copulations at a rate predicted fiom the fiequency of those shells inhabited in

the laboratory population. Males in Thasis daltoidea and Cvmatium spp shells were more

successful than expected, while those in Nerita sp. and Cinarîurn shells were less successful than expected. Their ability to execute precopulatory rotation of the females was negatively afYected by the round, open shape of the aperture and the angle of the columella to the plane of the aperture in both Nerita sp. and ~itt4um *a shells. The males were not able to grasp the females shells or rotate ?hem ~roperly.Also, males in those shells tended to !ose balance and fa11 over more fiequently during copulation atternpts than maies in Leucozonia, Thasis deltoida, or C;*matiui. The more ovoid and elongated apertures of Thasis deltoidea and Leucozonia shells allowed for easier execution of rotations and greater balance. For fernale C.tibicen, no significant difference was found in reproductive behaviour ammg individuak in different shd species.

Epibiotic growth on the outside of the sheli and the activities of other organisms living inside the shell can also affect the hennit crab (Conover, 1976). The growth of algae or anemones on the outside of the shell can severely damage it over tirne by weakening the shell structure and making the shell more fiagile (Jensen and Bender,

1973). Over time, a shell with extensive epibiotic growth may no longer be habitable for the hermit crab. However, anemones and hydroids can also be beneficial to the hennit crab by protecting it fiom predation (Ross, 197 1). Nereid woms (Taylor, 1979) and other polychaetes, copepods (Jensen and Bender, 1973), and porcellanid crabs (Telford and Daxboeck, 1978) sometimes inhabit the inside of the shell of some hennit crabs.

These associations are mostly detrimental, as the CO-habitantstake up space within the shell, may darnage the shell by boring (polydorids) (Jensen and Bender, 1973; Williams and Radashevsky, 1999), and in some cases may ingest the eggs and perhaps the larvae of females (Fotheringharn, 1W6a). As a hermit crab grows with each molt, it must ideally find a larger shell

(Markham, 1968; Fothenngham, 1976b; Bertness, 198 1c). Failure to find Iarger shells results in either the increased predation associated with inadequate shells or the inhibition of growth (Hazlett, 198 1). For some species, it has been shown that crab growth is slowed by occupation of a shell that is too small, even when excess food is present

(Fotheringh~rn,!976a). Sometimes, gowth can even be reversed (Markham, 1968).

Shells: A Limiting Resource

A lirniting resource is a required resource that constrains the population size of the species that relies on it (Rtcklefs, 1990). The size of the population is positively correlated with that of the resource; as the resource increases or decreases, the population size does the sarne. Many authors have suggested that gastropod shells are limiting resources, which restnct the size of hermit crab populations (Vance, 1972b;

Fotheringham, 1976b; Kellogg, 1976). The evidence presented are: (1) ernpty shells are rarely found in locations inhabited by hermit crabs (Provenzano, 1960). (2) empty shells added to sites are readily inhabited by hermit crabs, increasing the population density

(Vance, 1972b; Wicksten, 1977; BIackstone and Joslyn. 1984), (3) occupied shells are often severely damaged or of suboptimal size (Childress, 1972; Vance, 1972b) and (4) hennit crabs have evolved specialized behaviours that enable them to choose and cornpete for shells (Hazlett, 1966a).

Empty shells do not remain available for long time periods. They ofken become broken, buried, eroded (boring wonns and sponges), or otheMrise utilized by other organisms (anemones, calcareous algae) (Conover, 1976; pers. obs.). Under normal circumstances, hermit crabs cannot kill gastropods for theû shells (see Randall, 1964;

Rutherford, 1977, for exceptions). Therefore, the main source for shells in a population of hermit crabs is fiom other hermit crabs. These factors have led to shell exchanges and cornpetition for shells between individual hennit crabs of the sarne and of different species.

Competition and Shell Exchanges

Competition for shells between hermit crabs has sparked a controversy and debate in the literature. From early observations of the interaction between two hemit crabs, the behaviour was called a "shell fight" (Hazlett, 1966a). This implies aggression occumng where one individual is the winner of the interaction, while the other is the loser. With this came the terms "attacker" - hennit crab to begin the interaction, and "defender" - the opposing hermit crab. Since then, Hazlea (1978) has found evidence that supports the alternative concept of a "negotiation" strategy. There is no winner or loser in this situation, as both individuals benefit from the exchange. The hermit crabs are referred to as "initiator" and "non-initiator" to emphasize that the behaviour is not considered agonistic. The Hazlett negotiation strategy has been disputed by Elwood and Glass

(1981) and Elwood and Neil (1992), who present data that support the concept of an aggressive strategy. Whether hermit crabs are utilizing an aggressive or negotiation strategy, or perhaps both, conditionally, is still unresolved. The sequence of a typical exchange will be discussed here.

Competition begins when one crab approaches another. There is sometimes ante~alcontact, that can lead to (1) cheliped extension by one or both individuals, (2) retreat of one individual, or (3) one individual withdrawing into its shell (Dowds and

Elwood, 1983). In the third condition, the hermit crab that has not withdrawn examines the extemal features of the other's shell. This is accomplished as the examiner grasps the withdrawn crab's shell and uses its pereiopods to touch and rotate the withdrawn crab's shell. At this point, the examiner may either release the shell or continue investigation of the inside ofthe sheii. The sheli is now held by the pereiopods while the crab explores the inside and the aperture with one or both chelipeds. Experirnents conducted with glass shells did little to show what is happening inside the shell, although it appears that the hermit crabs are not in direct physical contact (Hazlett, I966a; Dunham, unpubl. data). In some instances, the examiner rocks the other's shell. Then, rapping occurs when the examiner's shell is moved against the withdrawn crab's shell (in Diogenidae) or the withdrawn crab's shell is moved against the examiner's shell (in Paguridae) creating an audible clicking sound. At this stage, the withdrawn crab is either pulled out (Dowds and

Elwood, 1983) or cornes out willingly (Hazlett, 1966a). The examiner continues to explore the vacant shell and may move out of its own shell and into the vacant shell.

When in the new shell, it will commence investigation of its old shell. It may retum to its old shell or retain the newly acquired shell. When the examiner either releases hold of one shell or moves away, the naked hennit crab that is left immediately inhabits the remaining shell.

Alternative Shelters

Aithough the Iiterature focuses on the use of spiral-form gastropod shells by hermit crabs, there are several species that utilize other cavities for shelters. Tusk, bivalve, and vermetid (tube-shape) shells, bryozoans, pieces of driftwood, bamboo, polychaete tubes, and cavities in corals, sponges, and stones are al1 used as shelters by hermit crabs (Table 1).

Alternative shelter dwellers are found in the families Diogenidae, Pyiochelidae

(Pomatochelidae), Paguridae, and Parapaguridae. They have yet to be found in the

Coenobitidae, although the cownut crab, Biraus latro, abandons sneii use altogether, hardening its abdomen soon after the glaucothoe larval stage (see Hartnoll, 1988, for discussion). The use of alternative shelters may have arisen independently in different groups or have evolved f?om a single common ancestor.

Since the initial descriptions of alternate shelter use, some of the hermit crab species involved have been studied further. The aspects of feeding (Markham, 1977;

Schu hmacher, 1977; Caine, 1980; Gherardi, 1994), agonistic behaviour (Caine, 1980;

Gherardi, 1996a), male-female pair formation (Patton and Robertson, 1980). intraspecific competition (Gherardi, 1996a), interspecific competition (Busato, et al., 1998), shelter exchanges (Gherardi, 1996a), protection from predation (Gherardi, 1996a), shelter choice

(Gherardi and Cassidy, 1994a; Gherardi, l996b), and larval and juvenile development and behaviour (Gherardi and McLaughlin, 1995; Gherardi 1996b) have received some attention.

Thus far, the only hypothesis as to why these hermit crabs would utilize other shelters has been proposed by Gherardi (1994; 1996% b) and Gherardi and Cassidy

(1994% b; 1995). They consider the alternative shelter dwellers to be descendents of spiral gastropod shell-dwellers and suggest that competition hmother hermit crabs has

Ied Discorsopamims schmitti to utilize polychaete tubes. Busato, et ai. (1998) also Table 1. Hermit crab species known to inhabit sheiters alternative to spiraled gastropod shells and the authors who first observed the association.

Hennit Crab Species Shelter Type Author, Year Superfamily Coenobitoidea 1 Family Pylochelidae (=Pornatocheiidae) 1 1 XIknown species of 1 Cylinàrical cavities in IForest.1987 Pvlocheles (Xvlocheles) and pieces of drifhvood Pvlocheles Bathycheles) Pylocheles Bathvcheles) incisus Tusk shells Forest, 1987 Pvlocheles (@locheles) anassizii Pieces of pumice stone; Forest, 1987; Forest et al., Pvlocheles ~Pvlocheleslmortensenii sponge, dead coral, 2000; Miyake, 1979 limestone Paraovlocheles scorpio Pieces of bamboo For- 1987 Cheiro~lateaspp. Cavities in sdlstones; Forest, 1987; Forest et al., sponges and btyozoans 2000 1 Chenoplatea mitoi 1 Calcareous rock 1 Miyake, 1979 I - Cancellocheles sculptiues Cavities in small stones Forest, 1987 Trizocheles boasi Within the interna1 tubular Forest, 1987 Trizocheles 1o~ua.x structures of thin walled Trizocheles caledonicus sponges Trizocheies brevicxulis Trizocheles pulcher Lithistid or haploscIerid Forest, 1987; Forest et al., TrizocheIes Spinosus spinosus demosponges that are 2000 Trizocheles Spinosus bathamae more massive than those above; purnice l

1 Trizocheles sakaii Tusk shells or serpulid Forest, 1987 tubes ( Pomatochefes iefFre~sii Tusk shells Miyake, 1979 1 Pomatocheles s~inosus Family Diogenidae CaIcinus tubularis Serpuiid worm tubes; Fenizia 1933; Zibrowius, vermetid tubes 1978 Calcinus verrilli Vermetid tubes Markham, 1977 CancelIus mayae Caicareous rock Forest et al., 2000 Caacel lus s~onpicola Cavities in sponges or Pope, 1953 calcareous Stones Paguristes barbatus Bry ozoans Taylor et al., 1989 Paguristes dieitalis Cavities in sponges Miyake, 1979 SuperfarniIy Paguroidea Family Paguridae Pamims sp. B ryozoans Taylor et al., 1989 Pwmsconstans Hydroid skeletons Miyake, 1979 Pagums imafiiki Tusk sheiIs Imafuku and Ando, 1999 Parmrus irn~ressus Sponges Sandford, 1995 Paaurus stevensae hide a sponge Hart, 1982 Pwritta corallicola iioles in corals McLaughlin and Lemaitre. Pmritta scottae 1993 Parniritta kroo~i Pamritta e;racilioes Polychaete tubes that are Schuhmacher, 1977 coral epibionts hritta harmsi Serpulid shells Gordon, 1935 Paguritta harmsi inside corals within Patton and Roberston, extended pits 1980 Paguntta moraani Worrn tubes and srnall McLaughlin and Lemaitre, holes in coral 1993 Discorso~aminisschrnitti Polycbaete tubes Pylo~apurusdiscoidelis Scaphopod shells Polychaete tubes Lemaitre and Campos,

Pvlo~apurusstewarti Bryozoans Taylor et al., 1989 Pylo~a~urussp. Luuhopaeunis (Lopho~agums) Bryozoans; tusk shells Taylor et al., 1989; Forest cookii et al., 2000 Lo~hopwnis(Looho~aeurus) Bryozoans Taylor et al., 1989 foresti Litho~ayrusycatanicus Holes in rock Provenzano, 1968 Rock-like sponges Xvlouami~stayrona 1 Cavities in pieces of wood I Lemaitre and Campos, 1993 Family Parapaguridae Para~apurusholthuisi 1 Anthozoans 1 Lemaitre, 1999 Para~apruslatirnanus 1 Zoanthids ( Lemaitre. 1999 Para~wrusbouvieri 1 1

Para~aaurusfùrici Paraoamrrus microps Scaphopod shells Lemaitre, 1999 Paraowrus richeri Paravaaurus saintlaurentae Zoanthids or actinians Lemaitre, 1999 Svm~amirusbrevipes Actinians Lemaitre, 1996 Svmpagums villosus

Svmpamirus dofleini Act inians Fautin-Dunn, et al., 1980 S~P~IUStrispuiosus Svrnpamrus dofleini Zoanthids Lemaitre, 1 994 Sp~aminisDaDposus Zoaathids Lemaitre, 1996 Svm~aminispoupini Actinians Lemaitre, i 994 Bivalvo~anurussinensis Bivalve shells with Lemaitre, 1993 actinians partialiy proteaing the abdomen Onco~amirusorientalis Zoanthids Lemaitre, 1997 suggest competition and resource partitioning as a way to explain the use of tubes by

Calcinus tubularis.

Hypotheses for the selective advantage of alternative shelter use by hermit crabs are:

(1) Gastropod shells are limiting. As previously described, gastropod shells are a

limiting resource that may explain the use of alternative shelters. A species that

utilizes novel shelters can eliminate the costs associated with interspecific

competition for shelten and must only deal with intraspecific costs.

(2) Alternative shelters eliminate or reduce the costs associated with shell dwelling. In

the case of sessile shelters (sponges, corals, and attached tubes), the energetic costs of

carrying a shell can be eliminated. Some shelters grow with the inhabitant (corals -

Patton and Robeason, 1980; sponges - Hart, 1982; bryozoans - Taylor et al., 1989)

or are easily modified by the hennit crab (driftwood - Forest, 1987), eliminating the

need to find new shelters as the animal grows.

To date, there is little information available about species that utilize alternative shelters. In order to obtain conclusive evidence for or against these hypotheses, it is necessary to understand the life histories of the hermit crabs as well as the positive and negative aspects of alternative shelter use for the hennit crabs involved.

Bermuda's Eademic Hermit Crab

The diogenid hennit crab Calcinus vemlli (Rathbun, 190 1) is one species that inhabits unusual shelters. It is the oniy hermit crab endemic to Bermuda (Provenzano,

1960), and can be found inhabiting both gastropod shells and gastropod tubes in equal numbers. The tubes are sessile and attached to reef substrate, while the shek are unattached and allow for mobility.

Calcinus vemlli's distribution between shells and tubes is unusual among the users of alternative shelters. The majority of alternative shelter dwellers do not use gastropod shells in the field at dl; individuals only utilize their alternative shelter. The natural use of traditional shelters (gastropod shells) by C. vemlli as well as alternative shelters (gastropod tubes) pmvides the ideal situation for studying the costs and benefits of alternative shelter use, and for investigating the bais of the decisions made by an individbal to inhabit one type over another. Other studies have had to artificially give half of their study animals gastropod shells in the iaboratory for cornparison (Gherardi,

1996a) or have made cornp~sonsto other species that solely utilize gastropod shells

(Gherardi, lW6b). Any study involving C. verrilli and the use of alternative shelters will not have these limitations.

Another important reason for studying C. vemlli is that it is an endemic species.

By definition, an endemic species is unique in that it is found in one area in the world and no where else (Cox and Moore, 1985). The main hypotheses for the existence of endemic species are that: (1) the species has evolved in adaptation to the environmental conditions of where it is found (see MacArthur and Wilson, 1967 and Pianka, 1978, for reviews), (2) the species has evolved due to genetic drift, usually because of a small population size, typical of the founder effect or a bottleneck in the population (see

Purves, et al., 1995, for a review), and (3) in the past, the species existed elsewhere and has since become extinct in al1 areas except where it is presently found (see Pieloy 1979, for a review). Broad evolutionary and biogeographic theory and more specific conservation and biodivenity issues, can be explored through studies of endernic species that lead to understanding the processes of speciation. Endemic species are also considered core elements of conservation programs as their iimited distribution, in itself, cm make them more susceptible to elirnination as a result of even localized habitat degradation. One basic element for such research is understanding life history traits of the endemic species. Despite its endemic status, few studies have concentrated on S. vemlli (see Chapter 1 for a review) and only one (Markham, 1977) began to investigate its shell- versus tube-dwelling lifestyle.

The present investigation focuses on the use of both traditional (shells) and alternative (tubes) shelters by Calcinus vemlli. The principal questions are:

(1) What is the present day distribution of C. verrilli in Bermuda, and which shelter types

are utilized in the five different marine habitats?

(2) How is C. vemlli distributed among the three types of shelters (one species of

gastropod shell and two genera of gastropod tubes) utilized in the field, and is this

preference a useful basis for predicting individual choice under laboratory conditions?

(3) Does cornpetition occur for gastropod shells between males and fernales?

(4) What are the morphologica1 differences between shell- and tube-dwellen, and can

morphology be altered with experimental manipulation of the shelters? CHAPTER 1

THE DISTRIBUTION OF CALCINUS VERR.ILLI IN BERMUDA

INTRODUCTION

Since its discovery in 1901, very few researchers have studied the biology of

Calcinus vemlli. From these studies (detailed below), there are fewer still that have

made contributions to the distribution of the species in Bermuda. Considering its status

as an endemic species, the primary objective of the present study was to determine the

distribution of C. vemlli in Bermuda. This was accomplished by: (1) conducting a review of al1 previous reports of C. verrilli in the literature, (2) thoroughly searching

previously recorded as well as potential new locations in the field, (3) determining the presence or absence of C. vemlli in these locations, and (4) recording the types of

shelters utilized by C. vemlli in locations where the species was found.

Previously Known Distribution

Rathbun (190 1) and Vemll(190 l), in separate reports, were the first to record C. vemlli nom Bermuda. They wrongly placed the new species in the genus Clibanarius, and VemH(1908) recognized the species as endernic to Bermuda. These early reports were based on a few preserved specimens.

It was not until 1960, that Provenzano placed the species in the correct genus,

Calcinus (see Ingle, 1993, for a key to Diogenidae), confirmed that it is an endemic

species, provided the first illustrations, and published the first records of the species' distribution in Bermuda (Figure 3). He found the species inhabiting Cerithium litteratum Figure 3. A map of Bermuda with the locations where Calcinus vemlli was found prior to and during the present study. Adapted from Stephenson and Stephenson (1972).

Legend: , sites where C. vemlli was found pnor to the present study; A , sites where

--C. vemlli was found both pnor to and in the present study; e, sites where C. vemlli was found in the present study; the land is shaded in light grey and the main reefs are outIined in black. shells (Born, 1778) at a variety of locations along the south and north shores of Bermuda and reported the approximate number found at the locations.

In 1965, Hazlett and Provenzano studied the behaviour of the glaucothoe and instar forms of C.vemlli within a larger, comprehensive study of the Diogenidae. Since the specimens of C. verriIli were only collected f?om plankton tows and ffom the

Challenger Bank iocated 25 km fiom Bermuda's mainland, very little information on distribution was obtained.

Markham (1977) discovered individuals utilizing sessile Dendropoma corrodens

(d'orbigny, 1842) and Dendropoma irrepulare (d'orbigny, 1842) vermetid tubes as shelters (most recent conserved names for Soiroelv~husannulatus and Soiroelvphus irrepularis, respectively [Turgeon et al., 19981). Because vermetid tubes are fixed to the substrate, the species could hold station in areas with constant surge, like intertidal areas along the south and nonh shores and the turbulent "boiler" reefs. He also found individuals inhabiting shells of C. litteratum although, like Provenzano (1960), did not find them in great numbers. In total Markham (1 977) recorded 19 individuals inhabiting shells from al1 locations he investigated.

In a study of recniitment at a reef site darnaged by a ship grounding, both Ç. litteratum and C. vemlli were found to be very abundant, compared to undamaged control sites, and replaced herbivorous fish as the dominant grazers on the reef (Smith,

1990). A complex chain of events led to the large population size of C. vemlli at the grounding site. The initiai impact of the tieighter in 1978, and the blasting that followed three months later to remove the wreck, created two types of disturbed reefs: (1) a completely flattened and defaunated area, with most reef structures destroyed, that encompassed an estirnated area of 0.44 km2 (Smith, 1985) and (2) a zone at the periphery of the completely disturbed reef. 25-50 m wide, that was defaunated but remained intact stmcturally. The loss of corals and reef structures resulted in a loss of topographie complexity. This, in tum, resulted in the loss of refuge for small- and medium-sized herbivorous fish. The populations of these fish were significantly reduced at the site compared to undamaged controls, while there was an increase in the number of predators observed, particularly barracuda (S~hyraenabarracuda). Herbivorous fish were absent and there was an increase in the growth of al1 expected algal species. The increased supply of food allowed for the colonization of the gastropod C.litteratum, whose shells provided for the subsequent colonization of C.vemlli. The gastropod and the hennit crab were found to pnmady forage on filamentous algae. Their 1-emoval of tilamentous algae allowed for the successful settlement of corai larvae and the beginnings of coral recovery at the site.

More recentiy, Campos and Lemaitre (1994) compared the morphology of C. vemlli to that of two other Calcinus spp fiom the Atlantic. The investigators used preserved specimens for their comparkons, of which the most ment specimen was collected in 1979. Therefore, the study did not add to our knowledge of the distribution of C. verrilli, although distribution was not an objective of the study. (Interestingly, they observed three specimens that had both male and fernale gonopores. One individual had a complete paired set of both, while the other two had paired male gonopores and a single fernale gonopore.)

The most complete records of the distribution of C. vemlli are between 20 years

(Markham, 1977) and 30 years old (Provenzano, 1960). Therefore, it was important to determine the present distribution of the species in Bermuda. In particular, 1 wanted to cobthe presence of shell-dwelling individuals, as significant numbers had not been reported in the literature, except at the ship grounding site. This was of importance because shell dwellers were essential for answering questions 2,3, and 4 posed in the

Introduction.

METHODS

Field investigations were carried out from May to Septernber, 1999, and Apd to

May, 2000, at the Bermuda Biological Station for Research (BBSR). 1 began by reassessing old sites investigated by Provenzano (196O), Markham ( 1977), and Smith

( 1990) and also examining previously unassessed sites.

In total 20 sites were visited and comprehensively searched (Figure 3).

Depending on the site, wading in tide pools, snorkeling, or SCüBA diving was required to observe animals. 1 recorded whether C. verriIli was present or absent, the shelter types available at the site, and the shelter types utilized by C. vemlli. Densities of Ç. vemlli were visually estimated at each site. Both the intertidal habitat and boiler reef habitat were only observed at low tide. Access to these two habitats was safer at low tide due to the higher waves and stronger currents at high tide. Al1 other habitats (subtidal, patch reef, and rim reef) were visited at both low and hi& tides.

Sites were distributed fiom the east end (St George's Parish) to the West end

(Sandys Parish) of Bermuda and cm be divided into five distinct habitat types. (1) The interiidal habitat is where numerous tide pools form in depressions at low tide. Durhg high tides, the entire area is submerged under 0.5-1 m of water. (2) The subtidal habitat does not usually exceed more than 2 rn in depth and is not exposed dunng low tides. (3)

"Boilers," which have the appearance of microatolls (diameter of 1-2 m), have a partially exposed surface at Iow tides (Morris et al., 1977). They are circular with raised rims that tend to be higher at the seaward side (Safiel, 1974). In Bermuda, the rim encloses a deeply eroded cup-shaped hollow. (4) Patch reefs are inshore reefs that cmbe found anywhere within the shallow lagoons of the Bermuda platform. They do not exceed depths of 3-4 m. (5) The rim reefs are found at the raised edge of the Bermuda platfom and extend inwards towards the lagoon, not exceeding depths of 9-10 m.

UPDATED DISTRIBUTION

My field surveys c~~rmedthe observations of Markham (1977) that C. vemlli occupies the tubes of both Dendro~omacorrodens and Dendropoma irremilare (which will be collectively referred to as "Dendropoma spp," since there is no diRerence in the structure of both tubes). 1 also found C. vedli commonly using the tubes of

Vermicularia spirata (Philippi, 1836) and Vermicularia knomi (Deshayes, 1843) (which will be collectively referred to as "Vermicularia spp," since there is no difference in the structure of both tubes) neither of which have previously been reporied as hennit crab shelters. The non-attached gastropod shell species used almost exclusively was C. litteratum. During the 7 months of field investigations, one individual each was found in

Cvmatium sp., Columbella mercatoria, and Conus sp. gastropod shells (for two of the snails, species was not detennined as the shells were highly eroded).

The Dendropoma spp tubes belong to the family Vermetidae (Safnel, 1975).

Vermetids are gastropods that have lost the snail form; instead their shells are loosely coiled, worm-like tubes that are either "welded" or embedded in the substrate. Some species are gregarious, which results in an aggregate ofclosely intercwined tubes. In

Bermuda, the two Dendropoma spp are small (diameter opening: 1.9-4.3 mm), prostrate and tightly coiled. They are embedded into the substrate, so that their openings are flush with the surface of the limestone. They use mucous webs to feed from the water column

(Safiriel, 1975).

The Vermicularia spp tubes belong to the fmily Tumtellidae (Gould, 1968).

Tunitelhds are a group of gastropods that are ciliary suspension feeders. A few of the rnembers are fkee living forms (genus Tumtella) that burrow into mud, apex dom, inclined at a steep angle to feed. However, the majority belong to the genus

Vermicularia, which, as juveniles, are coiled and orient thernselves in the substrate like

Tumtella. Vermicularia then attach to the substrate and uncoil in response to the availability of firm objects that provide a substrate for rapid growth (Gould, 1968). It is at this stage, when they are sessile and uncoiled, that the empty tubes are utilized by C. vemlli. In Bermuda, the Vermicularia spp tubes are slightly larger than Dendropoma spp

(diameter opening: 4.0-7.8 mm), more erect and more loosely coiled.

Calcinus vemlli was found to inhabit al1 of the five different habitats surveyed

(Figure 3, Table 2):

Interîidal Pool Habitat

The two sites investigated had tide pools that ranged greatly in size (0.25-10.0 m2) and depth (0.05-0.5 m). Calcinus. vemlli were oniy found in tubes located within tide pools (40 individ~als.m-~),never on the raised rims and areas between pools. The area Table 2. Sites visited from May to September, 1999, and Apnl to May, 2000, and the habitats and shelter types occupied by Calcinus vemlli.

Site Habitat Shells? Tubes? Method Collection site?

rock^ Bay 1 MSN* D wade Yes

Spittal Pond 1 M* D wde Yes

Achiiies Bay S no V snorkel no 1 Baileys Bay S no V,D snorkel Yes

--* Fort St. Catherine Beach S no V snorkel no

Gibbet Island S C V snorkel yes

Shelly Bay S no V,D snorkel no

WeBone Bay S no V snorkel no

Elbow Beach Boiler B no D snorkel no

Church Bay B. R C D SCUBA yes

Caricomp Seagrass North P C V* SCUBA yes

Crescent Reef I P C V* SCUBA yes

Crescent Reef 2 P C V SCUBA Yes

Tynes Bay East P no V SCiJBA Yes

Tynes Bay West P no V SCUBA Yes

Wreck Hi11 Reef P C V* snorkei Yes

Grounding Site R C D SCUBA Yes Hog Reef R C D SCUBA Yes

John Smith's Bay R C D SCUBA no

Twin Reef R C D SCUBA Yes

Legend: I, intem'dal; S, subtidal; B, boiier reef; P, patch reef, R tim reef; C, Cerithium litteraturn; M, Batillaria minima: N, Nerita tesselatta; D, Dendro~ornaspp; V, Vermicularia spp; *, the gastropod was present at the site but not occupied by Calcinus verrilii surrounding the opening of the tubes occupied by C. vemlli were heavily grazed and had very little algal growth. In some cases, red calcareous algae grew in the grazed areas, making the occupied tubes easily visible, because the surrounding area was composed entirely of brown filamentous algae.

Tubes occupied by the gastropods themselves @endropoma spp) xere found throughout the habitat, both submerged within pools and along the raised areas between pools. Empty Dendropoma spp tubes (not inhabited by either gastropod or hermit crab) were also found along the raised areas between pools, where the water had completely receded at low tide. However, the entire habitat would be tlooded at high tide, and al1 individuals within and between the pools would be submerged. No individuals, either gastropod or hermit crab were found above the high tide mark.

Spiraled gastropod shells, Batillaria minima and Nerita tessellata. species found in the intertidal habitat were occupied by the hermit crab, Clibanarius tricolor. Clibananus tncolor co-existed in the same tide pools as c. verrilii (although C. verrilli inhabited tubes there and not shells), but no interactions were observed between the species.

Calcinus vemlli was never observed in a gastropod shell in the intertidal habitat.

Subtidal Habitat

In this habitat, the shelter used most predominantly by C. verrilli was

Vermicularia spp tubes (15-20 individuai~.m'~).Vermicularia spp tubes inhabited by the gastropods were found throughout the sites investigated. None were observed above the low tide mark. No empty tubes were ever found; they were either occupied by the gastropods or the hermit crab.

At some sites classified as subtidal (Baileys Bay, Shelly Bay), Dendroooma spp tubes were inhabited by C. vemlli (1 5 indi~idua1s.m~~).Dendro~oma spp were not as common in subtidal habitats as they were in intertidal habitats. In subtidal, as in intertidal habitats, Dendropoma spp were observed up io the Iiigh tidz mark.

At the Gibbet Island site, four individuals inhabiting shells of C. litteratum were found. Living C. litteratum and shells occupied by the hermit crab Clibanarius tncolor were cornmon at this particuiar site but not at the other subtidal areas.

"Boiler" Reef Habitat

The microatoll formations are composed of biogenic matenal (to at least 5 m in depth below the reef surface) built by vermetids and coralline algae (Safnel, 1974).

Older vermetid and algal material is removed because of destruction by borers below the actively growing surface, and the hollows are filled in by a new growth of algae, foraminiferans, and serpulids, but not by vermetids. Therefore, the boilers are largely non-vermetid, although they are initiated and perpetuated by vermetids.

Any tubes not occupied by the gastropods were occupied by Ç. vemlli. The areas around the circumference of the opening were heavily grazed, but uniike the intertidal habitat, there was no red calweous algal growth. As also obsented by Safnel(1975), the raised rims of the boilers were heavily populated with Dendropoma spp (their tube openings were directly adjacent to one another, 100+ individuals.m"), the steep outside walls of the boilen were evenly populated (openings were approximately 2-5 cm from their nearest neighbor, 30-50 individualsm"), while the inner basins rarely had any

Dendro~omaspp present (10 individuals.m"). The distribution of C. verrilli on a boiler corresponded to the density of the Dendropoma spp observed.

At the Church Bay site, 1 utilized SCUBA to observe the base and sides of the four boilers located at the mouth of the bay. Calcinus verdi were also found inhabiting

-C. litteratum shells located around the base ofthe boiiers and along th& outer walls (10-

25 indi~idua1s.m'~)(Figure 4). No hemit crabs in shells were found along the raised nm of the reefor in the hollow basin.

Patch Reef Habitat

At these sites, C. vemlli were found in Vermicularia spp tubes and in Ç. litteratum shells. No empty tubes were observed; al1 were either still occupied by the gastropod or by S. vemlli (1 5-20 individua~s.m*~).Calcinus verriili in shells (5- IO individua1s.m") remained on the reef itself and were never found on the sand between reefs, although C. litteratum were sometimes found on the sand. Hennit crabs in shells were significantly larger in shield length at patch reef sites than at other sites (t = - 11.133, df = 147, P < 0.001).

Patch reef sites where C.vemlli were not found in Vermicularia spp tubes

(Caricomp Seagrass North, Crescent Reef I, and Wreck Hill Reef) did have VerrnicuIaria spp present. Despite this, on repeated visits during the summer of 1999 and spring of

2000,I did not observe any empty tubes, or any tubes occupied by C. vemlli. 4- 4- Seaward

High tide - Vermetids /

Low tide - Organogenetic - rock (aigae and dead vennetids)

Figure 4. A cross-section illustration of a "boiler" reef The black dots show the distribution of Dendroooma spp tubes inhabited by Calcinus vemlli on a typical "boiler" reef Adapted fiom Safnel(1975). Rim Reef Habitat

At the outer reef sites, C. vemlli was found in Dendropoma spp tubes (25-30 indi~iduals.rn-~)and CC.litteratum shells (1 0-1 5 individuals.mS2). Dendropoma spp tubes were located in dead coral heads as well as in limestone formations. At these sites, as on the boiler reefs, the areas surrounding the occupied Dendroporna spp tubes were grazed although they had no deposition of red caicareous algaz. Hennit ciabs in shells as well as live c. litteraturn were found al1 over the reefs, but never in the sand holes between reefs.

Another sympatric hermit crab species, Pamrus brevidactylus, was also found at the rim reefs and also occupied C. litteratum shells.

DISCUSSION

Desiccation and predation within habitats mon likely restrict C. verrilli. The hermit crab was either found below the low tide mark or in permanent pools above the tow tide mark, but aiways below the high tide mark. Without experimentation, it is not possible to distinguish between the negative effects of desiccation and predation on the distribution of C. vemlli.

From its distribution (found ody below the low tide mark), Vermicularia spp also appear to be vulnerable to desiccation, while Dendropoma spp are able to withstand at

Ieast the 1-2 hours when the tide is at its lowest point. Dendropoma spp possess a protective operculum that seals off the tube opening at low tide (pers. obs.) and most likely protects against desiccation. Vermicularia spp were not observed to seal off their tubes, although they do possess a thin opercuiurn (Sterrer, 1986). Rather, they withdraw further into their tubes when brought out of the water, a behavioural response that may not be as effective against desiccation as the seal of the Dendropoma spp operculum.

On the "boiler" reefs, hennit crabs in shells were not found along the rim or inside hollow. This distribution may partially be due to the effects of desiccation and partially to the force of the waves crashing over the reef at those points. These reefs were only observed at low tide due to observer safety pwzauiions (sce Methods). It is possible that durhg absolute high tide, when the effects of desiccation are lessened, hermit crabs inhabiting shells could migrate to the top of the boiler reefs, although this was not observed.

It is unclear why there were no S. vemlli inhabiting Vermicularia spp tubes at three patch reef sites. Although obsewations were made repeatedly over several months, none were ever observed, despite the presence of the tubes occupied by gastropods.

Because the tubes were in lower densities compared to other patch reef sites, any C. vemlli inhabiting tubes at these sites would be in correspondingly lower density (if the ratio of empty tubes to gastropod occupied tubes were the same). Therefore, they may have escaped detection.

Calcinus vemlli is very common and was found to inhabit every site and habitat type investigated. Because of its diverse use of shelters and wide range of habitats, C. vemlli rnay be the most common hermit crab in Bermuda. However, it was not the most common species at every site, where it sometimes came second to Clibanarius tncolor (in subtidd habitats) and Papurus brevidact~lus(on rim reef habitats). Since C.vemlli utilizes shelters other than the traditional gastropod shell, it is found in habitats that are inaccessible to the other two common hermit crab species in Bermuda. CHAfTER 2

SHELTER PREFERENCES IN THE ENDEMIC EERMUDIAN HERMiT CRAB,

CALCIMJS VERRILLI.

lNTRODUCTION

The majority of hermit crab species utiiize gasrropod sheils, wliiçli provide protection fiorn predation, physical stress and damage (Reese, 1969). The size and sh of gastropod shells influence both the growth (Markhain, 1968) and reproductive success

(Hazlett and Baron, 1989) of the inhabitant. Shell condition, along with size and shape, affect the hennit crab's wlnerability to predation (Vance, 1972; Bennes, 198 la).

Therefore, not only is a gastropod shell essential to the survival of most hermit crabs, the size, shape, and condition can also significantly influence the fitness of the hermit crab.

Even 6om the most casual observations, there appears to be a highly non-random association between crabs and the types of shells (Le. species, size, shape, and condition) they use. Early expenments sought to determine the most important shell dimensions being used by hermit crabs to select a particular shell over another. Weight (Reese,

1963) and volume (Benness, 1980) were suggested as the most important dimensions to the hermit crab. In order to increase predictability, investigators found that a combination of dimensions (weight, volume, length, width, aperture length and width) defining a certain "Gestalt," or used in a multiple regression, could more accurately predict shell use for some species (Kuris and Brody, 1976; Mitchell, 1976; Conover,

1978). Preferences have also been shown to be correlated with other shell variables, including the presence (Jensen, 1970; Conover, 1976) or absence (Wright, 1973; Grant and Ulrner, 1974) of hydroids on the shell, depending on the hermit crab species being tested. Species differences between gastropods, particularly related to shell size and intemal shape (Elwood, et al., 1979) and colour (Partridge, 1980), affect the choices made by a hermit crab. Past experience (Grant, 1963; Blackaone, 1954) and whether a shell has been previously used by a conspecific (Abmms, 1978) has been shown to be important for at least some species.

Preference is not static; it can change and be dependent on environmental conditions. Higher predation rates result in hermit crabs choosing heavier shells, with thicker apertures (Bertness, 1980; 198 1b, d; 1982). Hennit crabs that [ive in areas with high rates of water flow select significantly heavier shells than those conspecifics fiom still water sites (Hahn, 1998). In ares where the risk of desiccation is severe (high intertidal habitats), individuals prefer shells that have high spires, which retain more water than low spired-shells, and thereby minimize thermal stress (Bertness, 198 lb).

Despite the focus of research on the use of gastropod shells by hermit crabs, not al1 hennit crabs utilize gastropod shells. There are many species that use alternative shelters (Table 1), rather than "traditional" gastropod shells that are normally utilized by hermit crabs. Calcinus vemlli is a hermit crab that inhabits alternative shelters. It is unusual among the alternative shelter dwellers because it utilizes both gastropod shells and gastropod tubes in equal numbers, whiie mon of the alternative shelter dwellers do not use gastropod shells in the field. Therefore, it is an ideal species to use in midies of preference for "traditional" shelters (Cerithium litteratum shells) versus alternative shelters (Vermicularia spp tubes).

For Ç. verrilli, a choice made between Ç. litteratum shells and Vermicularia spp tubes results in drastically different life styles, due to the ecological differences that exist between the two shelters. In Bermuda, the gastropod shells are predorninantly found at rim reet but aiso at patch reefand boiler habitats (Chapter 1). The shells ;ire not atteched to the reef and so allow for mobility of the hermit crab. As they move they can feed by scraping algae and detritus off of the substrate. Presumably, shell exchanges and reproductive behaviour would occur and be similar to those observed in other hermit crab species (Hazlett, 1966a) although those behaviours were never observed in the field. Two other hermit crab species, Pamims brevidactylus (at the rim reefs) and Clibanarius tncolor (in intertidal and subtidal habitats), also utilize C. litteratum as their primary shell source (pers. obs).

Vermicularia knomi and Vermicularia spirata are predominantly found in subtidal and patch reef habitats in Bermuda (Chapter 1). The tubes are sessile and attached to the reef, so they do not allow for mobility of the hennit crab. The hermit crabs have been shown to filter small particles from the water column, using their pereiopods, which they extend from the tube opening (Markham, 1977). However, they are not restricted to this mode of feeding, as they also scrape algae and detritus fiom the surrounding substrate

(pers. obs.). The perimeter of the tubes are grazed of algae, suggesting that the hermit crab extends up to one body length from the opening to feed. Although it does not appear that they lave their tubes to feed, it is not known whether they leave their tubes to exchange shelters or to copulate (Markham, 1977). No other hennit crab species in

Bermuda has been observed to use the tube of either Vermicularia species as a shelter.

Ln order to investigate the preference of C.venilli for either C. litteratum shells or

Vermicularia spp tubes, 1 asked the following questions:

(1) What is the distribution of C. verrilli between these two shelter types observed in the

field'?

(2) What relationship exists between hennit crab size and shelter size, for both males and

fernales?

(3) What are the shelter preferences of C.vemlli in laboratory experiments?

(4) How does the distribution between shelter types determined in the field compare to

the choices made in the laboratory?

METHODS

This work was carried out in Bermuda fiom May to September, 1999, and Apnl to May, 2000, at the Bermuda Biological Station for Research (BBSR).

Fourteen of the 20 sites where C. vemlli was obse~edwere selected as collecting areas (Table 2). Depending on the location, wading in tide pools, snorkeling, or SCUBA diving was required to collect animals. Animals found in tubes were collected with a chisel and harnmer; those housed in shells were collected by hand. Individuals were isdated nom each other in partitioned plastic containers while in the field and in the laboratory, to ensure that shell exchanges did not occur.

Only S. litteraturn shells and Vermicularia spp tubes were offered in both the preference experiments, while Dendropma spp tubes were not. The main rasons for this were: (1) S. litteratum and Vermicularia spp tubes are more comparable in size and (2)

Dendroooma spp grow in complex aggregations, making it extremely dificult to know where one tube starts and the next one ends.

Al1 shelter dimensions were measured to the nearest 0.05 mm using vernier calipers. Shells were measured for length, width, and aperture length and width (Figure

9, whiie tubes were measured For opening diameter. Ail crabs were rmoved from :kir shelten in a similar manner: the tip of the shell or the base of the tube was broken with

Vice Grip brand pliers, and monofilament fishing Line inserted to gently urge the animal out. Sex was deterrnined with a dissecting light microscope at magnifications between lx and 1.5x and shield length (Markham, 1968), measured to the nearest 0.01 mm, at the same magnifications using an ocular micrometer.

Regression Analyses

A multiple regression was used to determine the correlation of the four shell measurements, and each was linearly regressed against shield length. The shell dimension of length was chosen as the variable to predict crab shield length, as it resulted in the highest correlation. Tube diarneter was regressed against crab shield length. Al1 animals were given back their original shelters and retumed to their collecting site. For al1 regressions, data for males and females were calculated separately. Regression analyses were conducted using SigmaStat software version 2.0 by Jandel. Regression

Iines were taken as indicative of preferred shell size by hennit crabs of a given size durhg preference experiments. Figure 5. A drawing of a shell showing the dimensions that were measured for the regression analyses. Adapted fiom Kellogg (1976). A, shell width; B, shell length; C, aperture length; D, aperture width. Preference Experiments

Animals used in preference experiments were not previously used in the . regression analyses. Pior to expenmentation, naked crabs (without shelters) were isolated for 24 houn in plastic cylindrical containers (diameter = 10 cm; height = 8 cm) with seawater, sand substrate, and compressed air. Only healthy, intact animais were used in the experimants.

1. Shelter Choice Experiment

Experimental set-up

The plastic isolation containers (see dimensions, above) were covered with a tiberglass mesh lid and 26 were submerged in a large glass aquarium supplied with a constant tlow through of unfiltered seawater from Ferry Reach near the BBSR, and maintained on the local (natural) light/dark cycle. Tumtellid tubes, Vermicularia knorrii and Vermicularia spirata, and gastropod shells, Cerithium litteratum, were obtained by collecting live individuais and sacrificing them with injections of sodium hydroxide so as not to damage the shells. These were washed and rinsed daily for three to four weeks pnor to being used in the experiment.

The preference of individuals for shells versus tubes was tested on a total of 95 hermits fiom one of four categories - 30 males collected in shells, 5 males collected in tubes, 30 females collected in tubes, and 30 females collected in shells. The sires ofthe shelters offered were determined by calculation fiom the respective regression line equation. One tube and one shell were placed next to each other on the substrate at the centre of the container. Once a hennit crab occupied a shelter, the individual's shelter occupancy was recorded every hour for the next four to six hours, followed by recordings made twice per day (at 1Oam and 2pm) for the next two days. Each crab was tested once and then returned to its collection site.

2. Chernical Choice Experiment

Apparatus and Materiais

A Y-maze was constmcted I~sing clear Plexiglas with two anns at a right angle to each other (15 x 6 x 10 cm, each) and with a base (19.5 x 6 x 10 cm) (Figure 6). The sand substrate was 1 cm deep and covered the bottom of the entire Y-maze. Inflow of non-filtered seawater into both arms was at a constant velocity of 0.5 cm.sS1and outflow was Grom the base. An open-topped removable fiberglass mesh cage (5 x 6 x 10 cm) was placed between the stem and two arms to prevent the crab fiom entering an arm when first introduced.

The extracts of mail chernicals from Cerithium and Vermicularia were prepared using a method simili: to that of Orihuela et al. (1992). From two to five gastropods were first placed on ice for approximately fifteen minutes. Removal of the soft parts

(whole animal excluding the foot and operculum) of the gastropods fiom their respective shells was accomplished using Vice Grip brand pliers and forceps. The tube and shell gastropods were placed into separate giass vials and frozen. The next day, the frozen tissue was ground, and weighed with an electronic balance to the nearest 0.1 g.

Unfiltered seawater was added in a ratio of 1 ml for each 0.1 g of snail tissue. The extract was removed and kept on ice throughout the day of the experiment. Each day, for the duration of the experiment fhsh samples of both extracts were prepared. Inflow

Hermit crab at start \ of trial

< / Removable mesh cage

Inflow

Figure 6. A drawing of the Y-maze apparatus used in the Chernical Choice Experiment. Prelirninarv tests

(1) As no previous study had tested hennit crab response to either Vermicularia spp or C. litteratum gastropods, 1 conducted tests to ensure that C. vemlli was able to detect both. A naked hermit crab was placed inside the open-topped mesh cage of the Y- mare. The extracts were prepared as described above and were introduced to the far end of one arm using a pipette. Mer 30 s the mesh cage was lified and the hemit crab was allowed to choose. Extracts were introduced to the Y-maze one at a time. The presentation arm was altemated and the maze was washed between trials. The test was repeated on a total of fourteen individuals, seven tested with Vermicularia spp and seven with C.litteratum.

(2) The use of the gastropod species as a potential food source by the hermit crabs was also tested. Both Vermiculana spp and C. Iitteraturn were tested. The gastropod was sacrificed and the entire body (without the shell) was placed with forceps at the center of the bottom of a IO-gallon tank (41 x 20 x 22 cm) containing 10-1 6 C. vemlli. The hermit crabs were observed and a11 behaviors were recorded. Two control stimuli were also tested: (1) a Stone (6 x 3.5 x 2 cm) was placed with forceps in the same position as the gastropods, and (2) the forceps were lowered into and raised out of the tank without leaving any object in the tank. The test of response to dl four stimuli (both gastropod genera and two controls) was presented in a11 of the four possible ordered combinations.

Each combination was repeated twice for a total of eight repetitions; fifteen-minute time intervals lapsed between the presentation of each stimuli within a repetition. Expenmental Set-Up

A naked crab that had been isolated for 24 hours was placed into the open-topped mesh cage of the Y-maze. Then, 0.5 ml of each gastropod extract was simultaneously introduced to the far end of a different amusing a pipette. Thirty seconds after extract introduction, the mesh cage was lifled and the following data recorded: (1) reached end of le&arm and exnact type, (2) reached end of right arm and extraci type, (3) remained in base, or (4) remained in the middle of an arm or no movement after 5 minutes. Food colouring and a digital stop watch was used to estimate the times required for the extracts to reach the fiberglass mesh cage, the midpoint of the base, and the end of the base.

These times were used to detemine when the mesh cage should be lifted (30 s after extract introduction) and the maximum time lirnit for the trials (5 min). The chemical choice experiment was performed on a total of 93 crabs, 30 fiom each of three categories

(males collected in shells, females collected in shells, females collected in tubes) and 3 males collected in tubes.

Following each trial, the Y-maze was washed thoroughly with eesh sea water and the substrate was redistributed. Cerithium and Vermicularia extract presentation arms were altemated between trials to eliminate any possible directional bias. Each animal was given the shelter it was originally collected in and retumed to its collection site.

Statistical Analysis

x2tests were calculated by hand; a table from Sokal and Ro hlf (1987) was used to determine P-values. Regression analyses, Student's t-tests (for nomally distributed data), and Mann-Whitney Rank Sum tests (for non-normal data) were calculated using Sigma

Stat software version 2.0 by Jandel. Significant P-values were those 5 0.05.

RESULTS

Field Observations

Calcinus vemlli were collected tiom 20 sites that represented five different habitats (Table 2). Measurements of animal shield length showed a significant difference between al1 males and females collected (Table 3). females being significantly larger than males. When the hennit crabs were grouped by shelter type, no differences were found in shield length between males and females collected in either Dendro~omaspp or

Vermicularia spp tubes (Table 3, Figure 7). However, the females collected in C. litteratum were significantly larger than the males from C. litteratum (Figure 7). When males and females from a single shelter type were pooled, individuals in Vermicularia spp were found to be significantly larger than those in C. litteratum (Table 3), while S. litteratum individuals were significantly larger than those in Dendropoma spp (Table 3).

The distribution of males and females among shelters showed significant differences (Table 4, Figure 8). Significantly more males than females inhabited C.

Iitteratum shells (x*= 34.68, df = 1, P 0.001), while more females than males were collected in both Vermicularia spp tubes (x' = 147.43, df = 1, P s 0.00 1) and

Dendropoma spp tubes (X' = 42-19. df = 1, P s 0.001). 43

Table 3. The statistical significance of shield length differences between Calcinus vemlli

males and females and shelter types, using (a) Mann-Whitney rank sum test and (b)

Student's t-test. P-values are considered significant at 50.05.

Hermit Crab N Median 25% 75% 1 Ail males 267 2.574 2.070 3.210

Al1 females 428 2.860 2.055 3.43 1

Dendro males 51 1,860 1.710 2.140

Dendro females 14 1 1.930 1.710 2.140

Centh males 201 2.717 2.2 10 3 -3 Cerith females 199 / 3.200 / 2.730 1 3.99

1 Ail Vermic 203 3.250 2.860 3.710

Al1 Cerith 300 2.890 2.305 3.520

Al1 Cerith 300 2.890 2.305 3.520

Al1 Dendro 192 1.926 1.710 2.140

Hermit Crab N Mean SD SEM T P

Verrnic males 15 3.324 0.648 0.167 0.354 0.724 Vermic fernales 188 3.262 0.650 0.0474

Legend: Dendro, Dendropoma spp; Centh, Cerithium litteratum; Vermic, Vermicularia

spp; N, sample size; 25%, 25" percentile; 75%, 75" percentile; SD, standard deviation;

SEM, standard error of the mean; T*,rank sum statistic; T, t-statistic; P, P-value. Males Females Males Females Males Fernaks Dendro~omaspp Vermicularia spp Centhium iitterahim

Figure 7. Calcinus verrilli shield length (mm) of males and females in the three different shelter types in the field. The bottom and top lines ofthe boxes give the 25" and 75h percentiles, respectively. The line through the box is the median. The bars below and above the box give the 10~and 90' percentiles, respectively. Table 4. The number of male and female Calcinus vemlli in the three types of shelters colIected in the field.

Shelter Males Females TOTAL

Cerithium 20 1 99 300

Vermicul aria 15 188 203

Dendro~oma 5 1 14 1 132

TOTAL 267 428 695 Males Females

Figure 8. The distribution of Calcinus vemlli males and females among three different shelter types in the field. Legend:O , Dendropoma spp tubes; , Vermicularia spp tubes; and H , Cerithium litteratm shells. Regression Analyses

A multiple regression of the four shell measurements that were recorded, shell length, shell width, aperture length, and aperture width, showed that they were correlated with one another (males: r = 0.928, n = 122, P s 0.001; females: r = 0.958, n = 34, P

0.001). Each shell measurement was linearly correlated with shield length for males and females (Table 5; for shell length see Figure 9, for sheil width, apenure iength and widtli see Appendix A, Figures 17- 19). The diameter of the tube opening was also correlated with shield length for males and females in both Dendropoma spp and Vermicularia spp tubes (Table 5, Figures 10-1 1).

Preference Experiments

1. Shelter Choice Experiment

An overall x2test conducted on choices made by males from shells, females from shells, males nom tubes, and females fiom tubes found no significant differences in shelter type selected (x2= 0.104,df = 3, P < 0.995) (Table 6). From observations made during the trials, the first choice that was made was not revened later. In the next 4-6 hours, and over the following two days, no individual was observed to have switched sheltets.

2. Chernical Choice Experiment

Preliminarv tests

(1) Individuals of C. vemlli were tested to determine whether they responded to

Cerithium and Vermicularia gastropod extract when only one or the other was introduced Table 5. Correlation coefficients obtained from linear regressions with Calcinus vemlli shield length, for each shell or tube measurement.

Hermit Crabs Measurement r

vlales in Cerithium sp. l length* 1 ippwidth i -0.847 1 aperture length 1 0.799 1 aperture width 1 0.8 14 - Females in Cerithium length* 1 0.877

width 0,797 33

aperture length 0.689 33

aperture width 0.759 33

Males in Vermicularia spp diameter* O. 844 6

Females in Vermicularia spp diameter* 0.644 1O8

Males in Dendroooma spp diameter* 0.3 57 40

Fernales in Dendropoma spp diameter* 0.430 76

I 1 1 I I Legend: r = coefficient of correlation; df = degrees of fieedom; * = measurements used to select appropriate shell and tube sizes for shelter choice experiment. Length = (9.068x SL) - 4.340

Hermit Crab Shield Length (mm)

Length = (9.549 x SL) - 4.5 15 / '/O @.

Hermit Crab S hield Length (mm)

Figure 9. The relationship between hennit crab (Calcinus vemlli) sire (shield length, SL) and shell (Centhium litteratum) iength inhabited by (a) males and @) fernales in the field. .O Diameter = (1.432 x SL) + 0.906 4' 4'

Hermit Crab Shield Length (mm)

.i Diameter =(LI19 x SL) + 1.661

Hermit Crab S hield Length (mm)

Figure 10. The relationship between hermit crab (Calcinus verdi) size (shield length,

SL) and Vermicularia spp tube opening diameter inhabited by (a) males and (b) fernales in the field. a Diameter = (0.678 x SL) + 1.683

Hermit Crab Shield Length (mm)

..a. *a Diameter = (0.666 x SL) + 1.573

Hermit Crab Shield Length (mm)

Figure 1 1. The relationship between hermit crab (Calcinus vemlli) size (shield length,

SL) and Dendroporna spp tube opening diameter inhabited by (a) males and (b) fernales in the field. Table 6. The choices made in the Shelter Choice Experiment between the gastropod shell, Cerithhm litteratum, and gastropod tubes, Vermicularia spp, by Calcinus vemili males and females collected in different shelters.

Sex and Shelter Collected In

Choice Males in Shells Females in Shells Males in Tubes Females in Tubes

Shells 14 i 8 3 13

Tubes 11 12 2 12 to the Y-maze. In al1 14 trials conducted, the hermit crabs moved down the arm of the Y- maze where the extract had been introduced, and did not rnove down the other m.

(2) Tests were conducted to determine whether C. verriIli was responding to the gastropod extract as a food source. When either the dead C. litteratum or Vermicularia spp gastropod was introduced to a group tank, there was an increase in movement of the hermit crabs. Rermit crabs thaî had been stationq kgan moviag, adthore that had been moving either changed directions or moved faster. Movement was not necessarily directed towards the dead gastropod in the center of the tank, as hermit crabs approached one another throughout the tank. When two (or more) individuals approached each other, behaviours associated with shell exchanging (General Introduction) occurred, although only one shell exchange was observed. In two instances, when a hermit crab reached the dead gastropod, the crab began to feed on it. However, in both cases when feeding occurred, it did not 1st for more than 60 seconds. The feeding appeared to be intempted, in each case, by another hermit crab approaching and initiating shell exchange behaviours. The same increase in activity was not observed when a Stone was placed into the tank, or when just a pair of forceps were lowered into, and then raised out of, the aquarium.

Experiment

An overall x2found a significant difference between extract choice and sex and the shelter collected in (x2= 8.62, df = 3, P < 0.05) (Table 7). This effect was due to femdes in tubes, which selected the Vermicularia spp extract significantly more often than the C. litteratum extract (x*= 6.5, df = 1, P < 0.05). Females in shells selected the Table 7. The choices made in the Chemical Choice Experiment between the gastropod

shell, Cerithium Iitteraturn, and gastropod tubes, Vermicularia spp, extract presentation

arms made Calcinus vemlli by males and females collected in different shelters. r Sex and Shelter Collected In

Extract Males in Shells 1 Femaies in Shells 1 Males in Tubes 1 Females in Tubes

Shells 16 20 i 8 I

Tubes 14 10 2 22 -C. litteratum extract slightly more often than the Vennicularia spp extract (x2= 1.67, df

= 1, P < 0.10).

DISCUSSION

Regression Analyses

Coefficients of correlation (r) rnay be îken as indices ûf shell size sxitability, since hermit crabs given fiee choice over time, tend to select shells of a certain size relative to their body size (Markham, 1968). The apparent difference in hermit crab size correlation between tubes and shells rnay be because selection pressure for individuals to have a snug-fitting sessile tube rnay be somewhat less than for a snug-fitting shell, which can be more easily carried than a shell that is too large. However, individuals in fixed tubes are also less mobile, and consequently have fewer opportunities for finding an ideal sized tube, which would also result in a lower correiation value.

Another possibility that could be explored firther and rnay explain the differences in correlation is mortality rates for tube gastropods rnay not be as high as for shell gastropods. Therefore, there rnay not be a large size range of empty tubes available for hermit crabs to occupy. There appears to be a greater size range of shells available (pers. obs.), suggesting that rnortdity is occumng amongst a variety of size classes of shell gastropods. This would result in a better match between hennit crab size and shell size, and therefore a higher r-value, while hennit crab size and tube size would not be as well comelated.

The observed differences in r-values for tube-dweuers versus shell-dwellers rnay be due to the shelter measurements chosen to predict crab shield length. By measuring four shell variables and showing their correlation with one another, 1 was able to choose the one with the most predictive value (Le. length). For both tube genera, diameter opening was chosen because it was the rnost accurate measurement that could be taken, considenng the methods used to retrieve the tubes from the reefs (chisel and hammer) and to remove the hermit crabs from the tubes (Vice Grip brand pliers). Measurements of tube volume or iength may have been more strongly comslated v;ith c;ab shie!d length, but as the tubes were broken during collecting and extracting the hermit crabs, neither of these measurements would have been very accurate.

Pnference Expenments

Males and females showed no significant discrimination between shells and tubes in the shelter choice experiment. Observations of the trials suggested that hermit crabs inhabited the first shelter that they approached. In many cases, one or the other of the shelters had not been obviously disturbed, so it may be that the individual never investigated both shelter types. None of the study animals ever changed fiom the shelter they initially selected, which suggests that they may not have made a true choice, as other species will usually "try onv7several available shells before making a final decision

(Hazlett, l966a).

Therefore, the experiment using chemical stimuli was conducted. In that experiment, I could be certain that each individual was exposed to both stimuli. The set- up was based on the studies of gastropod predation sites, where hermit crabs locate new gastropod shells from molecules released fiom gastropod flesh during predation events

(McLean, 1974; Rittschof, 1980% b; Rittschof, et al., 1990; Orihuela, et al., 1992). Hermit crabs have been shown to use chemical cues, followed by visual cues, to locate new shells from gastropods that are being predated upon (McLean, 1974). The chemicals are most likely peptides produced by enzymatic degradation of proteins (found to be

Trypsin) that originate nom gastropod flesh (Rittschof, 1980b). Hennit crabs have been shown to only attend sites containing gastropod flesh and are not attracted to other flesh sources, such as crustacean or bivaive muscle ksh(Rittschof, 1980a).

Since hermit crabs have been show to be attracted to specific species of gastropods and not to others (McLean, 1983). Prelirninary Test 1 was conducted. The results showed that individuais were able to detect both C. Iitteratum and Vermicularia spp extracts, and were attracted to them when they were presented separately. When both extraas were presented together in the chemical choice experiment, once again, males did not discriminate between C.litteratum and Vermicularia spp. However, for females, choice is linked to the shelter type they were collected in. Females collected in tubes showed a significant preference for the Vermicularia spp presentation arm, while females collected in shells showed a slightly signi ficant preference for the C. litteratum presentation am. This result is in agreement with the conclusions made by Grant (1963) and Abrarns (1978) that past experience is an important determinant of shelter preference.

As indicated by Preliminary Test 2, a choice made in the Y-mue towards one of the gastropod extracts does not necessarily correlate to a shelter choice for the hennit crab. In the preliminary test, two C. vemlli were observed feeding on the bodies of both

-C. litteratum and Vermicularia spp. This result is in agreement with reports from

Rittschof (MOa, b) that hermit crabs attracted to the source of the cues do not normally feed. Other observations have shown that hermit crabs do not eat gastropod flesh and will rip the flesh of a dead gastropod out of the shell, without feeding, in order to gain entry to it (Rittschof, et al., 1990). However, the preliminary test observations suggest that the choices observed in the Y-maze may be related to food, rather than to shelter preferences, perhaps for a minority of individuals. In either case, choice is biased by the shelter-type the individual was collected in, especially for females.

Diethism in Resource Utilization

Several workers have reponed a sexual diethism (exhibit different behaviour) in terms of resource utilization among difierent species of hermit crabs (Blackstone and

Joslyn, 1984; Asakura, 1995; Elwood and Kennedy, 1988). In each of these cases, males and females preferred shells of different species (Elwood and Kennedy, 1988, were the only ones to find these differences to be independent of size class), or restricted themselves to different size categories of the same shell species. Calcinus vemlli may be the only case thus far of a hermit crab exhibiting sema1 diethism in resource choice in which one sex prefers loose gastropod shells and the other attached gastropod tubes.

Asakura (1995) suggested a possible hypothesis to explain an observed gender difference in resource utilization. It relies upon males of the hermit crab species being significantly larger than their female conspecifics. Larger males tend to be better cornpetitors than femalcs, resulting in their ability to acquire greater numbers of available shells and greater numbers of the more preferred shells. This does not appear to be the case with C vemlli as females (in particular, females inhabithg C. litteratum) are significantly larger than males. The inverse of the same hypothesis, namely that females are out-competing males, is probably not occumng either, since males do not select the type of housing females predominantly use in the field, when given a choice.

A second hypothesis suggests that the housing difference is due to semai selection (Abrams, 1987). Among solely mobile gastropod-dwelling hermit crabs, successful males are reported as being larger than the females they mate with, as reproductive behaviour involves dragging and caqing the fernale (Hazlett, l966a), as well as mate guarding that has only been observed in Clibanarius vittatus (Hazlett, 1996).

In C. vemlli, most females are effectively sessile and therefore those behaviours cannot be involved in mating. Males do not need to attain a large size for access to females, while females can increase their reproductive output by growing, because they produce more eggs at a larger size (Hazlett, 198 1).

Cornparisons with Other Alternative Shelter Dweiien

Of the few studies that have investigated shelter preferences in hermit crabs that utilize alternative shelters, only one (Busato, et al., 1998) concemed a species (Calcinus tubularis) that naturaily uses both gastropod shells and tubes. Al1 other audies of shelter preference in alternative shelter-dwellers (Gherardi, 1996a, b; Imafiku and Ando, 1999) observed species that do not utilize gastropod shells in the field, although shells were offered as a choice in the laboratory.

Busato, et al., (1998) concluded that use by C. tubularis of alternative shelters is an example of "making the best of a bad situation," as the hennit crabs preferred mobile shells over sessile tubes, despite using both in the field. They suggested that tubes were used in the field to avoid interspecific cornpetition for shells. However, the authors did not compare the shelter type each individual was collected in when they recorded choice, and so it is not known whether previous experience may have affected laboratoiy choice.

My results for fernales are similar to those found by Gherardi (1996b), who observed that adults of Discorsopagurus schmitti prefer tubes to shells in the Iaboratory.

Discorsopagunis schrnitti is found exclusively in sabellarian tubes in the field. However,

-D. schmitti were found to prefer loose tub25 svzr sessile tubes, although loose tubs are not normally found in nature. Gherardi (l996b) found a difference in preference between juveniles and adults, with post-larval stages prefemng to settle into shells rather than tubes. Therefore, preference must change with developmental stage in o. schmitti.

Although this has not been tested in C. vemlli, it would make an interesting avenue for future research. The preference of C. vedi post-larval stages for either shells or tubes, rather than adult preferences. rnay be more important for determining the observed sexual differences in shelter occupancy that have been observed in the field. CBAPTER 3

INTRASPECTFIC SHELL COMPETITION IN THE ENDEMC BERMUDIAN

HERMIT CRAB, CALCINUS VERRlLLI

INTRODUCTION

Most hennit crabs must acquire shelis, because they provide protection from both predation (Reese, 1969; Vance, l972b; Bertness, 1982) and physical stress (Reese, 1969;

Shumway, 1978; Bertness, 1982). Inadequate shells (those that are too small, not the preferred species [i.e. shape], or considerably damaged) have been show to negatively affect reproductive success (Hazlett and Baron, 1989) and growth (Markham, 1968), and to cause the hermit crab to be more vulnerable to predation (Vance, 1972%b; Bertness,

198 1d; 1982). Shells are essential to the sunival of some hennit crabs and also directly affect their fitness.

Shells are also considered to be the limiting resource in most hermit crab populations (Vance, 1972b; Kellogg, 1976). The main evidence presented are based on field and laboratory observations: (1) available empty shells are rare (Provenzano, 1960),

(2) most hennit crabs occupy suboptimal shells (Childress, 1972; Vance 1972b), and (3) newly introduced shells are quickly inhabited by hermit crabs (Vance, L972b; Wicksten,

1977; Blackstone and Joslyn, 1984). Because of the limited supply of empty shells in most habitats, and the inability of hermit crabs to kill and acquire shells from living gastropods (see Randail, 1964, and Rutherford, 1977, for exceptions), the main source of a new or better shell for one hermit crab is fiom another hermit crab. Both interspecific and intraspecific cornpetition for shells occur in most crab populations. Interspecific competition has been the main focus of research on shell use. Since two or more species of hermit crabs can usually be found coexisting in intertidal and subtidal habitats and those species must utilize the same array of available shells, the question of coexistence is an interesting one (Scully, 1983a). Several studies have been conducted on assemblages of hermit crabs in diferent parts of the world (Vance, 1972b;

Grant and Uimer, 1974; Mitchell, 1976, Bach a al., 1976; Kellogg, 19%; Wang and

Jillson, 1979; Abrams, 1980; 198 la, b, c; 1982a; 1987; Bertness, 1980; 198 la, b, c, d;

1982; Gherardi, 1990; Busato, et al., 1998). Ln habitats where several species are sympatnc, a reduction of intenpecific competition is observed and has been attributed to:

(1) habitat partitioning - different species utilize diflerent parts of the habitat (Vance,

1W2b; Abrams, 1980; 1982a; 1987; Bertness, 198 1a, d; 1982; Gherardi, 1990),

(2) resource partitioning - different species utilize different shell species (Vance, 1972b;

Fothenngham, 1976b; Kellogg, 1976) or prefer different characteristics of the same

shell species, for example, prefenng shells with or without anemones (Grant and

Ulmer, 1974),

(3) differences in mobility and clumping behaviour, which have been observed between

direrent species, and result in a decrease in interspecific competition and an increase

in intraspecific competition (Gherardi, 1990).

Therefore, levels of interspecifïc competition are not as high as expected, and thus intraspecific competition has a significant impact on the shell supply of an individual

(Abrarns, 1987; Scully, l983b).

Intraspecific competition for shells among hermit crabs has not received as much attention as interspecific competition. Much of the work has focused on the diierent competitive abilities of males and females (Bertness, 198 1e; Asakura, 1995) and the effect of shell quality on the motivation to exchange shells, regardless of sex (Abrams,

1982b). In general, males have been found to be better cornpetitors than females

(Asakura, 1995; Bertness, 1981e), and non-ovigerous females have been found to be better cornpetitors than ovigerous females (Bertness, 198 1e).

ui the present audy, I investigata intraspècifiz cornpetition in Calcinus remlfi between males and females for the gastropod shell Centhium litteratum. This hennit crab species utilizes gastropod tube shelters (Dendrooorna irre-mlare. Dendroooma corrodens,

Vermicularia knonii, and Vermicularia spirata), as well as gastropod shells (C. litteratum) in the field. There is a sexual diethism in shelter use with more males inhabiting shells and more females inhabiting tubes (Chapter 2). The primary focus of the study is to determine whether cornpetition is a plausible explanation for the differential use of shelters by male and female C. vemlli. The questions I will address are:

(1) When males and females are matched by shield length, which sex gains access to

more shells?

(2) When females are 10% larger than males by shield length, which sex gains access to

more shells?

(3) How do major chela length and the presence of eggs affect the outcorne of contests

between males and females? METaODS

This work was conducted from April to May, 2000, at the Bermuda Biological

Station for Research (BBSR).

Hermit crabs were collected by hand from a variety of reef sites around Bermuda using SCUBA diving (Table 2). Only C.vemlli found sheltered in C. litteratum, a spiral gastropod shell, were used in this study. The animals wsre brought back :O the BBSR and maintained in group tanks with flow-through, unfiltered sea water. Each individual was only used in one trial, and was subsequently retumed to its original collection site.

Al1 hennit crabs were removed from their shells by breaking the shell apex with

Vice Grip brand pliers and using monofilament fishing line inserted into the broken end to urge the crab out. Any individuals visibly damaged by the procedure or already rnissing appendages were not utilized in any trial. The hermit crabs were sexed using a dissecting light microscope at magnifications between 10x and 15% and their shield length (Markham, 1968) and chela length (Figure 12) were measured to the nearea 0.01 mm using an ocular micrometer and a dissecting light microscope. A linear regression of chela length against shield length was calculated for males and females separately, using

Sigma Stat 2.0 by Jandel. For females, the presence or absence of eggs attached to the pleopods was noted.

Males and females were paired so that they were either (1) matched in size by shield length - fifteen pairs had equal shield lengths to 0.0 lmm and five pairs had < 5% dieerence in shieid length (in three of the five pairs, the males was larger; in two pairs, the female was larger), or (2) al1 females were at least 10% larger than males b y shield Figure 12. A drawing of the major chela of Calcinus verrilli, with arrow showing where measurements were taken. Adapted kom Campos and Lemaitre (1994). length. Al1 shells were damaged, so that the telson and uropods of the resident crab were clearty visible from the broken end of the shell.

Individuals were retumed to their respective damaged shells and isolated for 24 hours in cylindrical plastic containers (diameter = 10 cm, height = 8 cm) with fiberglass mesh lids, no added substrate material, and unfiltered sea water. Following isolation, the paired individuais were both inlroduced to opposite sides cf a nwel plastic container of the same dimensions that contained a sand substrate and unfiltered seawater. Animals were found to be very sensitive to any movements that occurred outside their holding tanks, so direct observation was avoided. Disturbances outside of the tank caused the hermit crabs to withdraw into their shells and stop moving. Therefore, in order to record behaviour accurately without an observer present, videotaping was employed. A 60-watt red light bulb was used to avoid the glue of the overhead halogen lights on the seawater.

It was positioned approximately 30 cm above the container.

The animals were allowed 10 minutes prior to recording to adapt to the darkened room, illuminated with oniy the red light illumination. Mer 10 minutes, the hermit crabs responded to shadows created over the container, suggesting that they had adapted to the illumination.

Intact and empty C. litteraturn shells ("good" shells) were obtained by collecting

Iive Ç. litteraturn and sacrificing them with injections of sodium hydroxide so as not to damage the shells. These were washed and rinsed daily for 3-4 weeks prior to use. The shell size used in a given test was determined by entenng the shield lengths of the animals used in the interaction into the equation for the regression tine of hermit crab size against shelter size (Figure 9). Both males and female shield lengths were entered into their respective equations; in al1 cases the larger shell length that resulted was used. The largest difference in shell size determined for the paired males and females was 1.26 mm.

Using a Sony Carncorder, the pair was videotaped for 5 minutes in a darkened room illuminated only with the red light. Mer the initial 5 minutes the "good" shell was introduced to the container. Videotaping continued for two hours, still in the dark with red light illumination. At the end of the two hours, the identit). of the occupant of the good shell was detennined (whether male or female). The pair was left undisturbed for a

24-hour period (videotaping was not conducted), after which tirne the occupant of the good shell was again determined. Any interactions observed while viewing the videotape were recorded. The same procedures were used for pairs that were matched by shield iength (n = 20), and those where the female was 10% larger than the male (n = 20).

Statistical Analysis

x2tests were calculated by hand; a table from Sokal and Rohlf (1987) was used to determine P-values. Significant P-values were those s 0.05.

RESULTS

Filrned Observations

During the initial five minutes of videotaping before the empty shell was introduced, usually both individuals moved around the container. In 36 out of 40 trials they encountered each other. In these cases, one hermit crab grasped the shell of the other and investigated the outside and inside of the other's shell. Investigation occurred as one hermit crab, using its pereiopods, held the other's shell and rotated the shell (with the occupant). Interna1 investigation of the shell began when one hennit crab prodded the aperture or the broken end of the other's shell vrith its pereiopods and chelipeds.

However, during the first five minutes, when both individuals were in damaged shells, no shell exchanges occurred. In none of the trials did it appear that there was diected rnovement of either individual towards the other. In 4 out of 40 trials, one of the individuals did not move around during the initiai five nhtés; in tbese cases, the mobile individual did not encounter the stationary one.

Once the "good shell was introduced to the container, movement of both individuals continued as before. Movement did not appear to be directed towards the empty shell. When one of the hermit crabs encountered the shell, it began to investigate both the outside and inside of the novel shell with its pereiopods and chelipeds, before occupying it. In al1 trials, the crab that first began to investigate the shell was the hermit crab that entered it. During the two hours of filming, shell exchanges did not occur between the new inhabitant of the "good" shell and the other individual in the trial. In three trials, the initial occupant of the "good" shell was eventually replaced by the other crab, during the subsequent 24 hours that followed videotaping.

Regression Analyses

Shield length was regressed against major chela Length for both males and females

(Figure 13). The regression equation for females was chela legth = -0.38 1 + (1.293 x shield length) (r = 0.948), while for males, the equation was chela length = -1.396 +

(1.728 x shield length) (r = 0.978). The two lines intenect at a shield length of 2-33 mm and a chela length of 2-63 mm. Therefore, at shield lengths < 2.33 mm, females have a O I 9 3 4 5 6 Shield Length (mm)

Figure 13. Linear regressions of Calcinus verrilli shield length (mm) against major chela length (mm) for males (solid line, filled points) and females (dashed line, clear points). larger major chela length than males, while at shield lengths > 2.33 mm, males have a larger major chela length than females.

Effect of Shield Length on the Contest

When males and females were the same shield length (Table 8a), males gained access to the "good" sheil significaritly inore frequefitltly than did fernales within the 2- hour observation time (x2= 7.2, df = 1, P < 0.01). Mer 24 hours, significantly more males than fernales were still occupants of the "good" shells (X2= 12.8, df = 1, P <

0.001). In 2 of the 20 trials, females who had obtained the "good" shell within the first 2 hours, exchanged it with the competing male wit hin the following 24 hours.

When females were 10% larger than males by shield length (Table 8b), no significant difference was found in the nurnber of males and females gaining access to the ernpty shell within the first 2 hours of videotaping (x2= 3.2, df = 1, P < 0.1). This did not change aAer 24 hours (x2= 1.8, df = 1, P < 0.5). In 1 of the 20 trials, a male exchanged shells with a female and thereby gained occupancy of the "good" shell within the subsequent 24 hours.

Effect of Major Chela Length on the Contest

When al1 pairs (those matched by shield length and those where females were

10% larger than males) were pooled (Table 9a), a significant effect of major chela size was found on the outcorne of the contest in the first 2 houn (x2= 16.21, df = 2, P <

0.001). In al1 trials where males had a larger major chela than fernales, the males were more likely to occupy the shell in the first 2 hours (x' = 10.89, df = 1, P < 0.00 1). When Table 8. The resuIts of shell cornpetitions (a) between male and female Calcinus verrilli of the same shield length and (b) between C. verdi females that were 10% larger than males, at 2 hours and 24 houn after the introduction of a "good" shell.

(a) l Winner of "Good" Shell Male i Femaie / TOTAL 1

2 hours 16 4 20

r Winner of "Good" Shell

Mate Female TOTAL

2 hours 6 14 20

24 hours 7 13 20 Table 9. The results of shell cornpetitions between male and female Calcinus vemlli, when males have a larger major chela than females (M > F), females have a larger major chela than males (F > M), and males and females have equal major chela lengths (M = F), at (a) 2 hours and (b) 24 hours after the introduction of a "good" shell.

(a)

r l Winner of 'Goo8" Sheii 1 Male 1 Female 1 TOTAL

TOTAL 22 18 40

Winner of "Good" Shell

Female females had a larger major chela, they were more likely to occupy the empty shell (x2=

5.56, df= 1, P < 0.025). In the 4 trials where male and female major chela lengths were equal, the number of male and female winners were also equal. Overall, either sex is equally likely to obtain the "good" shell in the first 2 hours, if they have the larger major chela within a pair (x2= 0.8, df = 1, P < 0.5).

Mer 24 hours (Table 9b), thsre were aiil a significant eEect of majcr che!a size on the sex of the winner (x2= 20.33, df = 2, P < 0.00 1). Signi ficantly more males inhabiting the "good" shell when males had the larger major chela (x2= 18, df = 1, P <

0.00 1). In the trials where females had a larger major chela than males, there was a slightly significant difference between the sexes inhabiting the "good shells (x*= 3.56, df= 1, P < 0.1). Mer 24 hours, there was no change in shell occupancy in the 4 trials where major chela sizes were equal between males and females. There is an indication that males are better than females at maintaining shell possession after 24 hours, even if they did not have the larger major chela within a pair (x' = 5.8 1, df = 1, P < 0.025).

Ef'fects of the Presence of Eggs on the Contest

The results of al1 40 trials were pooled to determine the effect of females with and without eggs on the outcome of the contest (Table 10% b). Within the first 2 houn, there was no difference in the outcome of the contests when females were ovigerous versus non-ovigerous (x' = 0.6, df = 1, P

"good" shells with their respective males. Table 10. The results of shell cornpetitions between male and female Calcinus vemlli when females were ovigerous (Ovig) or non-ovigerous (Non) at (a) 2 hours and (b) 24 hours after the introduction of a "good" sheli. (4 Winner of "Good" ShelI

Male Femaie TOTAL

Ovig 12 12 24

Non 10 6 16

TOTAL 22 18 40

Winner of "Gooà" Shell

Male FemaIe TOTAL

Ovig 13 12 24

Non 12 4 16

TOTAL 25 16 40 DISCUSSION

Regression Analyses

The regression analyses suggest that there is a sexually dimorphic allometry in major chela length Males have a greater chela length to shield length ratio than females, when shield length is longer than 2.33 mm. This is not unusual among hennit crabs;

Biackstone j 1385j found Paprus loneicarpus males [O have a grsater major chela Iength relative to females.

Exploitation and Interference

Cornpetition can be divided into two categories, exploitation and interference.

With exploitation, the competitor gains access to the resource by being more efficient at obtaining that resource (Miller, 1967). For hermit crabs, this translates into finding and inhabiting an empty shell. In the present study, exploitation competition occurred in the first two hours of the male-female interaction. There was an empty shell present that could be potentially exploited by either individual.

Interference occurs when the competitor increases its own supply of the resource, by direct rernoval of the resource Eom its cornpetiton (Miller, 1967). Although empty shells do occur in nature, shells are more fiequently acquired through interference competition. In hermit crab interactions, the best example of interference competition is shell exchanges. Interference competition in the present study could potentially occur after one of the individuals in the interaction occupied the empty shell. The set-up allowed 24 hours for interference to occur. The present expenmeni has found that males are better exploitation competitors than females, when both sexes have the same shield length. This is in agreement with the results of Asakura (1995), who studied the hennit crab Diogenes nitidimanus. Male o. nitidimanus were thought to be better competitors than females because of sexual selection for larger sizes in males. Larger males were more successfÙl than smaller males in mating with females. It was not determineci whether this was due to male-male cornpetition, female choice, or both (Asakura, 1995). The most successful competitors for shells in the population also mated most fiequently with females. Asakura (1995) found that for females, size was not related to mating success, although female fecundity was not considered in the study.

Sexual selection for larger sue in males does not apply to C. vemlli, as females inhabiting the gastropod shell Ç. litteratum were found to be significantly larger in shield length than males inhabiting C. litteratum (Chapter 2). However, even when males were paired against females that were 10% larger, males were still able to win half of the exploitation encounters. Females did not gain access to significantly more shells than did males, despite being larger. This suggests that some other variable, besides shield length, is a better predictor of the outcome of contests between males and fernales in C. vemlli.

Predicting Contest Outcornes

By pooling al1 the trials that were previously divided into either pairs matched for shield length or pairs where females were larger, the effects of extemal eggs and major chela size on the outcome of cornpetitions between males and females could be analyzed.

The presence of eggs on the pleopods of females involved in contests did not appear to affect the results of those contests. There was no difference in the sex of the winner when a female was ovigerous versus non-ovigerous. This is different fiom the results of

Bertness (198 le) who found that males were better competitors than non-ovigerous fernales, and non-ovigerous females were better competitors than ovigerous females. The most direct test of the effect of extemal eggs on the outcome of an encounter would be to

pair non-ovigerous and ovigerous fernales. Howevrr, bassd on the present data, &ere

seems to be no effect on either exploitative or interference competition in C. vemlli.

There is a significant effect of major chela size on the outcome of competition.

When compared by major chela length, males and females are equal in their exploitative

abilities. Most females with the larger major chela were able to gain access to

significantly more shells than males dunng exploitation competition, although one female with the Iarger chela lost the "good" shell in interference competition. Two males with larger chelae gained the "good shell in interference competition from their competing

females that they were unable to access in exploitation cornpetition. Therefore, there is the indication that males are better than females at interference competition, a larger

sample size is necessary to coniïrm this result.

In trials where pain were matched so that females were 10% larger by shield

length than males, the major chela length of the fernale was not necessarily larger than that of her competing male. Since the proportion of individuals with the larger major

chela length were nearly equal in the trials where females were 10Y0 larger by shield

length, there was no significant difference in the sex of the winner when females had a

larger shield length than males. Ln Ç. vemlli, success in shell competition is best

predicted with major chela length and shield length. CHAPTER 4

THE EFFECTS OF SHELTER TYPE ON UROPOD SYMMETRY IN CALCINUS

VERRILLI

INTRODUCTION

The hennit crab body form is unusual in cornpanson tu the other members of the

subphylum Cmtacea. It has been highly modified for shell utilkation, with an asyrnrnetrically coiled abdomen, and reduced size as well as structural complexity of the

4~ and 5' pereiopods, telson, and uropods (Figure 1). The shape of the particular shell that a hermit crab inhabits can further influence the specific shape of the individual.

Crabs in shells with narrow apertures tend to have a greater degree of dorso-ventral flattening than conspecifics in shells with wide apertures (McLaughlin and Bailey-Brock,

1975). Papnis lonnicarpus was found to attain a smaller size in high-spired shells, than

low-spired shells. This was attributed to the smaller intemal volume in high-spired shells compared to low-spired shells (Blackstone, 1985). The major chela of some species

conforms to the shape of the shell aperture, which makes a more effective block of the shell opening (Blackstone, 1985). Paprus loneicarpus males in the high-spired shells

had a longer major chela than those males in low-spired shells which was attributed to the

longer and more narrow aperture of high-spired shells compared to the shorter and wider

aperture of low-spired shells.

Further evidence for the direct effect of the gastropod shell on herrnit crab

morp hoiogy has been presented by Harvey (1 998). Individuals of Clibanarius vittatus

had asymmetrical uropods at the first juvenile (megalopa) stage. In order to test the maintenance of asyrnmetry, groups of laboratory-reared megalopae were either given a

shell to settle into or were given no shelter. The initial asymmetry increased in the

sheltered juveniles, while those without shells became more symmetrical. Although asymmetry appeared in that species initially, it was strongly affected by residence in a

shell.

Some hermit crabs cio not utiiize coiied gastropod shriis for slielters, but acquire

alternative shelters (Table 1). Alternative shelters are typically tubes of polychaetes or

gastropods, or cavities in sponges, corals and rocks that are relatively unifonn in diameter over the fil1 Iength of the shelter. The hermit crabs that utilize these alternative shelters

have slight morphological differences from the typical hermit crab form: (1) the abdomen of species that use alternative shelters is usually straight, rather than coiled (Selbie, 192 1;

Gherardi and Cassidy, 1994a), and (2) the uropods are symmetrical, rather than asymmetrical (McLaughlin and Gunn, 1992; McLaughlin and Lemaitre, 1993; Gherardi and Cassidy, 1994a; Gherardi and McLaughlin, 1995; Imafuku and Ando, 1999).

The asymrnetricd abdomen of hermit crabs is generally believed to be due to the asymmetrical, coiled gastropod shells that most occupy. Therefore, rnorphological

departures from this asymmetry have been regarded as secondary adaptations to life in an

alternative shelter (Hazlett, 1969; Barnes, 1986; Gherardi and Cassidy, 1994a).

However, there is no expenmental or phylogenetic evidence for the hypothesis

(McLaughlin and Lemaitre, 1997), only correlations between symmetry and alternative

shelter dwelling. Also, the results of one study (Gherardi and McLaughlin, 1995) suggea

that not ail hermit crabs have similar morphological responses to their shelters, or similar

morphological plasticity. Discorsopa_mims schmitti, a hermit crab that exclusively inhabits uncoileci, syrnrnetncal sabellarian tubes in the field, was laboratory reared for the study (Gherardi and McLaughlin, 1995). The species was observed to have symmetrical uropods as both an adult and a megalopa (last larval fom preceding the crab stage).

Individuals at the first adult molt were given tubes tu inhabit, shells to inhabit, or no shelter. Only uropod orientation (those in shells had flexed uropods, those in tubes had uropods closely pressed against the abdomen) was azected by sheitzr, while uropod symmetry and pleopod asymmetry were the same in al1 treatment groups. For this species, habitation of tubes did not result in a change towards uropod symmetry, since the uropods were symmetrical during the megalopal stage, prior to settling into a shelter.

Therefore, the lack of uropod morphological plasticity offers no support for the former hypothesis.

Gherardi and McLaughlin (1995) have been the only investigators to attempt to manipulate uropod symmetry in alternative shelter-dwellers. In the present study, I investigate the effect of shelters on the uropod morphoiogy of C. verrilli, a hennit crab endemic to Bermuda, which utilizes both gastropod shells and gastropod tubes in the field. Calcinus vemlli is ideal for this kind of study, as cornparisons of morphological symmetry and asymmetry can be made among different field populations and among experimentally manipulated laboratory groups. The questions 1 asked are:

(1) What observable differences are there in uropod morphology between tube- and shell-

dwellers?

(2) Can shelter manipulations change uropod morphology? METHODS

This work was carried out from January to March, 2000, and June to July, 2000, at the University of Toronto and fiom Apd to May, 2000, at the Bermuda Biological

Station for Research (BBSR).

Individuals of C. vemlli were collected from various reef sites in Septernber and

December, 1999, in Bermuda and transporteci to the Ramsay Wright Zoologka1

Laboratories at the University of Toronto. Depending on the location, wading in tide pools, snorkeling, or SCUBA diving was required to collect animals. Animals found in tubes were collected with a chisel and hammer; those housed in shells were collected by hand. In both the field and while in transit, they were maintained in large 1-gallon plastic bags a quarter-filled with seawater, in groups of 20 to 25 individuals. Animals collected in shells were kept separate from those collected in tubes, to be certain that shelter exchanges did not occur between groups, and so that recent shelter history for each animal was known. Although never observed, exchanges within groups may have occurred. In the laboratory in Toronto the crabs were maintained in IO-gallon aquariums

(40 x 20 x 22 cm) with grave1 substrate, an under-grave1 filter system, compressed air, and artificial seawater (Instant Ocean brand), maintained at a salinity of about 35 ppt.

Each aquarium contained between 20 to 25 individuals with the same shelter type. The crabs were fed every second day with Trout Chow (Purina). The environmental room was maintained at 27'C on a 12: 12 lightldark cycle. Field Observations

Vice Grip brand pliers were used to remove hermit crabs from their respective shelters, by cracking the apex of the shell or the base of the tube, and then inserting monofilament fishing Iine into the shelter to urge the hermit crab out. Once naked, hermit crabs were sexed with a dissecting light microscope and measured with an ocular micrometer. The shieid iength (@Iarkham, 1968) and length of the left nght urcpods

(Figure 14) were measured to the nearest 0.0 1 mm. The direction the abdomen coiled, whether left or right, was also recorded.

Asymmetry Indices (AI)

Asymmetry indices are a comparative measure of asymmetry. The asymrnetry index is AI = (L-R)/(L+R); L and R refer to the left and nght uropod lengths, respectively

("left" and "right" were defined from the perspective of the hermit crab). It ranges on a scale from -1 to 1. When AI = O, there is perfect symrnetry, i.e. there is a difference of

~0.01 mm between lengths, the uropods of the left and right sides are equal. Convenely when AI = -1 or 1, there is perfect asymmetry. The length of the lefi or right uropod, respectively, is not measurably different fiom zero. Negative values for AI occur when the nght side is longer than the left, while positive values indicate that the lefi side is longer.

Shelter Manipulation

In order to determine the possible effects of shelter type on hermit crab morphology, the shelten were manipulated. Crabs collected in shells were oEered the Figure 14. Drawings of the lower abdomen of Calcinus vemlli Eom (a) a shell and (b) a tube. The letters refer to the same parts on both: LU, lefi uropod; 4 abdomen; RU, right uropod; and T, telson. appropnate size tube for their shield length, as ascertained fiom regression equations

(Figure 1 1). These will be referred to as "forced tube-dwellers." Individuais collected in tubes were given an appropriate size shell (Figure 9). Those collected in Vermicularia spp tubes will be referred to as "forced shell-dwellers-V," white those collected in

Dendropoma spp tubes will be referred to as "forced shell-dwellers-D." Once in their new shelter, the hermit crabs were maintainèd in the aquariums as before. h order to accuratety collect and record the molts of each crab, each individual was isolated in a plastic mesh cube container (5 x 5 x 5 cm) with a hinged !id, which was subrnerged in an aquarium.

Each day the hermit crabs and their containers were checked for newly molted exoskeletons ("molts"), which were recorded and removed. At least 2 days post-molt (to allow for hardening of the exoskeleton) the hermit crab was removed fiom its shelter, as described above, and the shield length and left and nght uropod lengths were measured with a dissecting light microscope and ocular micrometer to the nearest 0.01 mm. The crab was returned to the same shelter unless the shelter was badly darnaged due to the

Vice Grip pliers, in which case a new shelter of a similar size was offered. In either case, the crab was returned to the plastic mesh container in the aquarium.

For April to May 2000, the hermit crabs were transponed to the BBSR where the experiment continued unintempted. The animals were maintained in the same isolation containers as described above, in an aquarium filled with unfiltered seawater aerated with compressed air. They were fed every other day with processed fish food. Molt checks and measuring continued as before. In June, 2000, the sarne animals were transported back to the University of Toronto, where maintenance was the same as before. They remained in Toronto for the completion of the expenrnent. Each hennit crab was followed until July 3 1, 2000.

Statistical Analysis

Student's t-tests, paired t-tests and one-way ANOVAs (for normally distributed dataj or Mann-Whitney rank sum tests, Ranked sign tests and Krtiskal-Wallis One-way

ANOVA on ranks test (for non-normal data) were calculated using Sigma Stat software version 2.0 by Jandel. A pairwise multiple cornparison procedure using Dunn's Method was used when a significant difference was found with an ANOVA rank test (Sigma

Stat). Significant P-values were those < 0.05.

RESZILTS

Field Observations

Asymmetry indices (AI) of left and nght uropod length were calculated for individuals collected in the gastropod shell Cerithium litteratum, vermetid tubes

Dendropoma irreeulare and Dendropoma corrodens, and tumtelid tubes Vermicularia s~irataand Vermicularia knomi. A Kniskal-Wallis one-way ANOVA on ranks test found a significant dserence between the AI'S of shell dwellers and both types of tube dwellers (H = 94.0 1, df = 2, P 5 0.00 1) (Figure 15). A pair-wise multiple cornparison procedure, using Dum's methoci, found significant ciifferences (P < 0.05) between shell dwellers and both types of tube dwellers. No significant difference was found between the AI'S of both types of tube dwellers. The abdomens of a11 individuals, regardless of Cerithium Vermicularia Dendropoma litteratum spp Tubes spp Tubes S hel1s (n = 26) (n = 26) (n = 85)

Figure 15. Box plots mmparing the asymmetry indices of shell and tube dwellers of

Calcinus vemlli in the field. The bottom and top lines of the boxes give the 25' and 75" percentiles, respectively. The line through the box is the median. The bars below and above the box give the 1 and 90& percentiles, respectively. shelter type, coiled to the right. For al1 individuals where the uropods were not perfectly symmetrical, the left uropod was aiways longer than the right.

Shelter Manipulations

There was a change in the absolute left and right uropod lengths for forced tube- dwellers, forced sheli-dweilers-V, and forced sheii-dweiizrs-D over consecutive molts

(Table 11).

The forced tube-dwellers showed a decrease in Ai's over four consecutive molts

(Figure 16a). A Paired t-test found a significant difference between the pre-molt and first molt AI'S (t = 5.247, df = 24, P 5 0.00 1). A Kmskal-Wallis one-way ANOVA on ranks test found a significant difference between the Al's of the first, second, third, and fourth molts (H = 8.757, df = 3, P = 0.033). A pair-wise multiple cornparison procedure, using

Dunn's method, found a significant difference (P < 0.05) between the first and third molts only. Al1 other pair-wise cornparisons were not significant.

Forced shell-dweIIers-V showed an increase in their AI'S over three consecutive molts (Figure 16b). A Paired t-test found a significant difference between the pre-molt and the frrst molt AI'S (t = -5.309, df = 18, P 1 0.00 1). A one-way ANOVA found no significant differences between the AI'S of the first, second, and third molts (F = 1.6 13, df = 24, P = 0.222).

Forced shell-dwellers-D showed a sirnilar increase in AI'S over three consecut ive molts (Figure 16c). A Ranked sign test found a significant diEerence between the pre- molt AI'S and the first molt (W = 23 1, n =2 1, P < 0.001). A one-way ANOVA found no Table 11. The mean lefi (L) and nght (R) uropod lengths (mm) of Calcinus vemlli forced tube-dwellers, forced shell-dwellers-V, and forced shell-dwellers-D over consecut ive molts. Molt I 1 Molt 2 1 Molt 3 1 Molt 4 Pre-Molt I

Forced tube- dwellers

Forced shell- dwellers-V

Forced shell- dwellers-D Pre-molt Molt 1 Molt 2 Molt 3 Molt 4 (n = 25) (n = 25) (n = 17) (n = 9) (n = 3)

Figure 16. Box plots of the asymmetry indices for Calcinus vemlli that were (a) forced tube-dwellers, @) forced shell-dwellers-V, and (c) forced shell-dwellers-D over several molts. The bottom and top lines of the boxes give the 25' and 75" percentiles, respectively. The Iine through the box is the median. The bars below and above the box give the 10" and goLhpercentiles, respectively. Pre-Molt Molt 1 Molt 2 Molt 3 (n=20) (n=19) (n=5) (n=2)

Pre-molt Molt 1 Molt 2 Molt 3 (n=21) (n=21) (n= 12) (n=2) significant differences beîween the AI'S of the first, second, and third molts (F = 0.6 13, df = 34, P = 0.548).

The final AI'S recorded (whether molt 1, 2,3, or 4) for forced shell-dwellers-V or

-Dand forced tube-dwellers were not signi ficantly di fferent from field shell-dwellers and field tube-dwellers, respectively (Table 12).

DISCUSSION

Field Observations

Calcinus vemlli field shell-dwellers were found to have uropod AI'S similar to other gastropod shell-dwelling species (Imafuku and Ando, 1999). Field tube-dwellers, regardless of the tube species they inhabited, had almost perfectly symmetrical uropods.

The results for tube-dwellers are similar to the uropod AI'S for the alternative shelter- dweller, Papums imafukui calcuiated by Imafùku and Ando (1999) and as observed by various investigators of other alternative shelter-dwellers (McLaughlin and Gunn, 1992;

McLaughlin and Lemaitre, 1993; Gherardi and Cassidy, 1994a; Gherardi and

McLaughlin, 1995).

When the uropods of C. vemlli were not perfectly symmetrical, they were always left biased (lefi was longer than right), regardless of shell dwelling or tube dwelling. The abdomen always coiled to the right when individuals were naked. These are characteristics of more traditional shell dwellers, which suggest that C. vemlli may be a descendant of a shell-dwelling ancestor, most likely one that inhabited dextrally coiled shells. Further evidence for a shell dwelling ancestry is that ody 4 of the 33 known Table 12. Cornparison of the final asymmetry indices (AI'S) for Calcinus vemlli forced dwellers at the end of the laboratory expenment with the AI'S of the respective shelter dwellers in the field. Calculated with (a) Student's t-test and @) Mann-Whitney rank sum test.

(a)

Sheiter "LY Mean SD SEM T

Shell (forced Vermic) 19 0.218 0.054 0.0123 -1 .O32 Shell (field) 85 0.236 0.676 0.00733

S helter N Median 25% 75% T*

Shell (forced Dendro) 21 0.250 0.223 0.285 1264.5 Shell (field) 85 0.240 O. 180 0.280

Vermic(forcedshel1) 24 0.035 0.000 0.055 595 ,O 26 0.040 0.000 0.060

Legend: Shell, Cerithium litteratum; Vermic, Vermicularia spp.; Dendro, Dendroporna spp.; T, Student's t-statistic; SD, Standard deviation; SEM, Standard error of the rneans;

T*, Mann-Whitney statistic; P, P-value; 25%, 25" percentile; 75% 75" percentile; N, sample size. species of Calcinus are alternative shelter dwellers; the rest inhabit spiraled gastropod shells (Morgan, 199 1).

Shelter Manipulations

Over the course of the experiment, both groups of forced shell-dwellers became more asymmetricai in uropod lenyth, witli the most drastic change in asymmetrj occumng at the first molt. The uropods of the forced tube-dwellers became more symmetrical throughout the experiment. There was a significant diflerence between the pre-molt and the fust molt AI'S of the uropods, and there was another significant difference between the first and third molts. This suggests that in the case of the forced tube-dwellers, symmetry is not achieved in one molt. but gradually attained over several.

This contrasts with both groups of forced shell-dwellers who had asymmetrical uropods after their first molt.

The different rates of change to uropod symrnetry or asymmetry between forced shell-dwellers and forced tube-dwellers may be due to differential use of the uropods among the groups. Govind and Pearce (1986) found that differential use of chelipeds by lobsters induced claw asymmetry. The chela that was exercised more developed into the crusher claw, while the other became the cutting claw. A simiIar expIanation may apply in the case of differential rates of uropod changes in asymmetry and symmetry in C. vemlli.

Rough pads on the end of each uropod (Barnes, 1986) likely function to hold ont0 the inside of the herrnit crab's shelter. Since shells are carried around by the herrnit crab, the uropods of shell-dwellers are "exercised" more than those of tube-dwellers because the tubes are sessile. The greater use of the uropods by shell-dweilers, when compared to tube-dwellers, rnay explain the differential rate of uropod change between those forced into tubes versus those forced into shells.

Another possible explanation for the difference in the rates of change of the uropods is that, developmentally, it rnay be easier for reduction in size and structure to occur, rather than for gowth of appcndagzs. Grouth or re-goavth of appendzges in decapods usually takes more than one molt; for example, the growth of the snapper claw in snapping shrimp takes two molts to be complete (Mellon and Stephens, 1978). In terms of hermit crab uropods, it may be easier to change from symmetrical to asymmetrical uropods by reducing the size of the right uropod (as in forced shell- dwellers), while asymmetrical to symmetncal changes require several molts to increase the size of the right uropod (as in forced tube-dwellers). There may be greater metabolic costs involved in increasing the size of a structure, cornpared to reducing a structure.

From the point of view of the tube dwellers, there may be benefits associated with more symmetncal uropods. Contrary to the findings of Gherardi and McLaughlin (1995) with o. schmitti, the uropods of Ç. vemlli are fanned out within the tube (pers. obs.), most likely to secure the animal within the shelter. It follows that symmetrical uropods anchor the hermit crab inside the tube more successfully than asymmetrical ones, since the tube is relatively circular in cross-section.

In al1 cases, the final uropod AI'S of forced shelter-dwellers did not differ fiom the field individuals inhabiting the same types of shelters. Through shelter manipulation only, 1 was able to alter the uropods of C. vemlli so that they closely matched the uropods of field individuals in the same shelters. Therefore, for C. vemlli adults, shelter type has a significant effect on uropod symmetry. This may be the first experimental evidence of an alternative shelter affecting symmetry in a hennit crab species. An earlier study on the hennit crab Calcinus vemlli reported the use of the attached tubes of the vermetids, Dendropoma corrodens and Dendropoma irregulare as shelters, along with the more "traditional" loose gastropod shells typically used by other hennit crabs (Maridiam, i377j. From fieid investigations, I have faund that C. vemfli also inhabits the sessile turritellid tubes of Vermicularia s~irataand Vermicularia knomi, alternative shelters that have not been recorded previously as hermit crab shelters.

Shelters other than the coiled gastropods are referred to, generally, as alternative shelters.

These discuveries led to the focus of the present study, which was to investigate the use of different shelters by C. vemlli, a hermit crab endemic to Bermuda.

Field Surveys

Calcinus vemlli was found inhabiting al1 five of the different habitat types surveyed, including intertidal pool, subtidal, "boile?' reef, patch reef, and rim reef habitats, at twenty different sites (Chapter 1). Because of its diverse use of shelters and wide range of habitats, C. verrilli may be the rnost comrnon shallow water hermit crab in

Bermuda. A number of the habitats in which it is found are inaccessible to the two other comrnon hennit crab species in Bermuda, Clibanarîus tncolor and Parnirus brevidactvlus.

Semai diethism of shelter use was found dunng field surveys. More C. vemlli males inhabited the shells of Cerithium litteratum, and more females inhabited the tubes of Dendrooorna spp tubes and Vermicularia spp tubes. A significant diflerence in shelter use between male and fernale hermit crabs is rare (Blackstone and Joslyn, 1984; Asakura, 1995; Elwood and Kennedy, 1988) and only in one previous case was the difference shown to be independent of size (Elwood and Kennedy, 1988). Calcinus verrilli may be the only hennit crab known thus far to exhibit a sexual diethism in resource choice, in which one sex is predominantly found in loose gastropod shells, while the other is in attached gastropod tubes.

Preference for Shelters

In order to detemine whether the differences in shelter use of C. litteratum shelIs and Vermicularia spp tubes between males and females were due to preference by one or both of the sexes, two experiments were conducted (Chapter 2). In the first experiment, naked hermit crabs were allowed access to both types of shelters over a 24-hour penod.

No significant discrimination was made, regardless of whether the crab was male or female, or had previously occupied a shell or tube. Observations of trials suggested that the hermit crabs were not aware of both shelters, and so could not have made a choice, as they inhabited the first shelter that was approached and never changed shelter occupancy in the two days that followed each trial.

The second preference experiment used a Y-maze and chernical stimuli from the gastropods of each shelter type. It was designed to ensure that each hennit crab was exposed simultaneously to both stimuli. Males did not discriminate between the extracts of C.litteratum and Vermicularia spp, regardless of shelter type previously occupied.

However, for females, choice was linked to the shelter type they were collected in.

Females collected in tubes showed a significant preference for the Vermicularia spp presentation arm, while those in shells showed a slightly significant preference for the Ç.

litteratum presentation m.

Although the results of the preference experiments show that females are more

likely to choose shelters based on prior experience, this does not explain why there are

proportionately more females inhabiting tubes over shells, i.e. why their pnor experience

is biased towards tubes. The results for maies show that they do not discriminata between the gastropod extracts, although they can detect both extract types when

presented separately (Chapter 2, Preliminary Test 1). Therefore, the chemical choice

experiment shows that it is not a simple difference in attraction to these two gastropods

by adults that determines the distribution of males and females observed in the field.

However, the two preference experiments do not exclude the possible importance of

choice in shelter occupancy.

When hermit crab eggs hatch, the larvae are released fiom the female pleopods,

and then spend most of their developmental stages in the plankton (Pike and WiIIiamson,

1959). The glaucothoë (young crab stage) is the first stage to enter shelters (Agassiz,

1875). Therefore, it is possible that the choice made by the glaucothoë of C.vedli

while selecting their first shelter is important for determining the observed later

distribution of adult males and females between shelters. The continued shelter

preference of the adult hermit crabs could be influenced by the initial choice made by the

young crab stages. Without some ef5ect of the glaucothoë shell preference on adults, any

differences in seleaion made by the glaucothoë would not be maintained in the adult

population. Cornpetition for Shelters

Another possibility is that the differences in shelter use observed between males

and females are due to competition. In Chapter 3,: investigated exploitation and

interference competition between males and females for Ç. litteratum. hdividuals of the

diEerent sexes were paired so that they were either matched by shield length or females

were 10% larger than males by shieid iengrh. Boh individuals in a pair occupied

damaged shells and competed for one "good (undamaged) shell. During the first two

hours of the interaction, exploitation competition or the efficiency at finding an empty

shell was tested. Once the shell was occupied, interference competition or the ability to

keep versus obtain the "good" shell was tested. When males and females were matched

by size, maies won significantly more than females did at exploitation competition, while

there was no difference in interference competition between the sexes. When females were 10% larger than males, there was no significant difference between the number of male and female winners. Therefore, shield length is not the only determinant of the outcome in a shell contest.

The presence of eggs on the pleopods of females did not affect the results of the contests. Females with eggs were not any more likely to win or lose a competition than those without eggs. However, there was a significant effect of major chela size on the outcome of competitions. The individuals within the pairs with the Iarger major chela won significantly more in exploitation competition, regardless of sex. Therefore, both major chela length and shield length are important determinants of the outcome of a shell contest between males and fernales. The cornpetition expenment explains why females in C. litteratum sheils were found to be significantly larger than males in Ç. litteratum (Chapter 2). Previous studies with other hennit crab species have found males to be significantly larger than females

(Asalcura, 1995), perhaps because of their mating behaviour, where males must grasp and rock the shell of females (Hazlett, 1966a). in C. vemlli, large females have a smaller major cheia than maies with the same shiéld Iéngth. Therefore, there is 3 dimorphic allometry in major chela length between the sexes, with maies having a greater major chela length to shield length ratio than fernales. Because of this dimorphism, and because major chela length and shield length together, rather than just shield length, better predict cornpetitive success, only the largest females are able to inhabit and remain the occupants of C. litteratum shells. Furthemore, these large female occupants of C. Iitteratum are significantly larger than the male occupants. In al1 other shelter types @endropoma spp and Vermicularia spp gastropod tubes) in which C. verrilli is found, no significant difference in shield length exists between males and fernales. Therefore, in order to compete adequately with males for shells and shell retention, females in C. litteratum shells must be larger than their conspecitic males for a given shell size.

A Polydorid Affecting Shelter Use

The observed diethism in shelter use between male and female Calcinus vem*lli may be associated with one or both sexes avoiding the costs of one shelter, by living predominantly in the other. For males, the costs of living in a sessile tube are probably higher than those associated with mobile shells. Males that are mobile will have an advantage over males that are sessile in terms of finding food and new shelters for growth, and obtaining copulations and being reproductively successful. The costs of being in a tube are probably quite similar for females as they are for males. Despite these costs, fernales are predominantly found in tubes. It is possible that, for females, there are other costs associated with sheli-dwelling rnaking the sum greater than those associated with tube-dwelling.

Hennit crabs are nor the only inhabitants of Ç. litteratun gastropod shells. I have observed a new polychaete species in the genus Polvdora, living inside the shell, close to the apex (Appendix B). It is not unusual for polydorids to inhabit gastropod and bivalve shells (see Sato-Okoshi, 1999; and Williams and Radashevsky, 1999, for reviews) and a number of other species of polydorids have been reponed living with several other hermit crabs species inside gastropod shells (Brightwell, 195 1; Jensen and Bender, 1973;

Fothenngham, 1 W6a; Dauer, 199 1; Williams and McDermott, 1997; Williams and

Radashevsky, 1999).

Fotheringham (1976a) has shown that the polychaetes have access to the brood space within the shell and that several species will readily eat the hennit crab eggs and larvae offered to them in the laboratory. Egg consurnption rates indicated that if eggs are brooded for as long as one week, a single Pol~doraindividual could consume several hundred eggs from each brood. I have observed the unidentified Polydora sp. inside a C. litteratum shell with a berried C.verriili female. The wom had herrnit crab eggs inside its gut.

In Bermuda, no polychaete was found inhabiting any of the gastropod tube species utilized by C. vemlli, and there are no known reports in the literature of polydorids inhabiting gastropod tubes. For C. verrilli females, the high costs associated with egg-loss due to a Polvdora-inhabited shell, cm be eliminated by living in a tube.

Therefore, for fernales, tubes may be the shelter conferring selective advantage through avoidance of egg and larval predation. For males, shells may be the default better option, with the advantages that mobility confers.

Morphological Differences

As a final cornparison of shell- versus tube-dwellers, I investigated morphological differences in the uropods of both groups (Chapter 4). Shell-dwellers, like most other hermit crabs, were found to have asymmetrical uropods, while tube-dwellers had more symmetrical uropods. In order to determine whether the shelter influenced these differences, some individuals collected in tubes were given shells, while some individuals collected in shells were given tubes.

The experiment showed that the morphological differences between the uropods of tube- and shell-dwellers were environmentally controlled by the shelter. This may be the first experimental evidence of an alternative shelter affecting symmetry in a hermit crab species. The abdomen always coiled to the right, regardless of shelter, and if uropod lengths were diflerent, the left was always longer than the right, strongly implying a shell-dwelling ancestry, specifically one that utilized dextraily coiled shells. APPENDIX A

REGFUSSION ANALYSES FOR GASTROPOD SHELL MEASUREMENTS AND

CALCINUS VERRILLI SHlELD LENGTH

Hennit Crab Shield Length (mm)

Width = (3.243 x SLI + 2.4 14

Herrnit Crab Shield Length (mm)

Figure 17. The relationship between hermit crab (Calcinus vemlli) size (shield length,

SL) and shell (Cerithium litterahim) width inhabited by (a) males and (b) females in the field. Shell Aperture Length (mm) Shell Aperture Length (mm) a

Apemire Width 1.167 x SL) + 0.557

Hennit Crab Shield Length (mm)

a ,' y*'% O* Aperture Width = (1 .O22x SL) + 0.904

Hermit Crab Shield Length (mm)

Figure 19. The relationship between hennit crab (Calcinus verrilli) size (shield length,

SL) and shell (Cerithium litteratum) aperture width inhabited by (a) males and @) femdes in the field. APPENDIX B

A NEW POLYDORA SP. (SPIOMDAE, POLYCHAETA)FOUND INSIDE THE

GASTROPOD SHELLS OF CALCINUS VERRILLI

Dunng the present study on Calcinus verdi, the tube- and shell-dwelling hennit crab, I found a polychaete inside the sheiis oFCerithiurn litteratum with the hennit cnb.

It was identified as belonging to the genus Pol~dora(Spionidae) (P. Pocklington, pers. corn.), making it the first record of Polvdora in Bermuda. It has yet to be identified to species. Individuals were observed eating the fecal pellets of C. verrilii and one individual was found with hermit crab eggs in its gut. An estirnated 40-50% of shells with hermit crabs contained single specimens of Polvdora sp. It is not known whether the woms bore through the shell to gain access like some other species of polydorids (Sato-

Okoshi, 1999) or enter through the shell aperture (Brightwell, 195 1).

Like other members of Polydora, individuals inhabit burrows or tubes inside of the gastropod shells on the shell wall that are most likeIy self-excavated (Sato-Okoshi,

1999). Polydorids are known for invading calcareous substrates, like gastropod shells, bivalves, coralline algae, and barnacles. Some species of worms are considered pests, as they burrow into commercially important shellfish, and so have been well studied

(Williams and McDermott, 1997). Several are recorded as cohabiting with hermit crabs, including Polydora ciliata with Parnirus bemhardus, Polydora neocaeca with Pa.gums loneicamus. Polvdora websteri with Clibanarius vittatus and Polydora comrnensaiis with both Parnirus annulioes and Payrus pollicarpus (Jensen and Bender, 1973;

Fothenngham, 1976a; Dauer, 1991; Williams and Radashevsky, 1999). The relationship between hermit crab and polychaete has been mainly studied from the point of view of the polychaete (Williams and McDermon, 1997). The polychaete benefits f?om its association with the hemiit crab by obtaining food particles that have been (1) suspended in branchial currents and (2) dropped by the hermit crab during feeding. From the point of view of the hermit crab, there do not appear to be any obvious benefirs, aithough there are some definite costs. The polychaete etetakes up spzce inside the gastropod shell that could be occupied by more eggs and they have been shown to feed on both hermit crab eggs and larvae (Fotheringharn, 1 976a). Therefore, for female hermit crabs, the negative effects of an association with a polychaete rnay be very costly. REFERENCES

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