DISCRIMINATION OF CHEMICAL SIGNALS FROM GASTROPODS BY HERMIT CRABS

by

Deirdre C. Gonsalves

A Thesis Submitted to the Faculty of

The College of Science

in Partial Fulfillment of the Requirements for the Degree of

Master of Science

Florida Atlantic University

Boca Raton, Florida

August 1996 Discrimination of Chemical Signals from Gastropods by Hermit Crabs

by

Deirdre C. Gonsalves

This thesis was prepared under the direction of the candidate's thesis advisor, Dr. William R. Brooks, Department of Biological Sciences, and has been approved by the members of her supervisory committee. It was submitted to the faculty of The College of Science and was accepted in partial fulfillment of the requirements for the degree of Master of Science.

SUPERVISORY COMMITTEE: dAJLrtuiL Thesis Advisor -1//A~ ~ ~~4p~

s and Research Date

11 Acknowledgements

I would like to thank Dr. Randy Brooks for his guidance, assistance and faith in me as a graduate student and researcher. He is truly a role model for all aspiring scientists.

Thanks to my committee members, Dr. Sheldon Dobkin and Dr. Alex Marsh for their significant contributions to the manuscript. I would also like to thank Drs. Dan Rittschof and Mike Salmon for their creative comments and ideas. I owe an enormous debt of gratitude to Patty Baechler for her assistance in crab collection and maintenance and

George Jones at Gumbo Limbo Marine Lab for his help in maintaining hermit crab tanks.

Special thanks to the love of my life, Craig Campbell Jackson who now knows more about hermit crabs than most psychologists care to know. Lastly, thanks to my aunt,

E. Yvonne Irving who supported me in all my endeavors and instilled in me the importance of education and laughter. This work was supported by a grant from the

National Science Foundation to Dr. William R. Brooks.

ill ABSTRACT

Author: Deirdre C. Gonsalves

Title: Discrimination of Chemical Signals from Gastropods by

Hermit Crabs

Institution: Florida Atlantic University

Thesis Advisor: Dr. William R. Brooks

Degree: Master of Science

Year: 1996

Some species of hermit crabs can locate chemically predation sites where snails are consumed and subsequently obtain their shells. This study addressed four questions: 1) Is chemotaxis to snail odors prevalent among hermit crabs? 2) Do members of hermit crab lineages respond similarly to common snail odors? 3) Do hermit crabs respond more acutely to snails whose shells they most frequently occupy? and 4)

Does phylogeny of snails influence responses by hermit crabs? Two sets of congeners

(C/ibanarius vittatus/ C. tricolor and Dardanus venosus/ D. fucosus) in the family

Diogenidae, and three congeners (Pagurus pollicaris, P. longicarpus, and P. annulipes) in the family Paguridae were tested. Fifteen species of snails from 11 families served as test odors. Hermit crab response was measured by the fondling display, where one hermit crab investigates the shell of a neighboring crab. The diogenids discriminated odors more readily than did the pagurids. Correlations between responses and shells most frequently occupied existed for C. vittatus and D. venosus. Clibanarius tricolor was the only crab to respond to confamilial test odors.

IV \ Table of Contents

Acknowledgements ...... iii

Abstract ...... iv

List of Tables ...... vi

List of Figures ...... vii lntroduction ...... 1

Materials and Methods ...... 4

Hermit crab and snail species ...... 4

Crab maintenance ...... 5

Extract preparation and experimental apparatus ...... 8

Experimental procedure ...... 8

Results ...... 10

Diogenids ...... 10

Pagurids ...... 11

Discussion ...... 26

Prevalence of Responses ...... 26

Patterns of Responses within Hermit Crab Lineages ...... 28

Shell Occupancy Patterns and Responses ...... 29

Snail Phylogeny and Responses ...... 30

Conclusions ...... 31

References ...... 32

v List of Tables

Table 1. Odors presented to hermit crabs during bioassays to test for shell­

investigative or fondling behavior Most odors were extracts from

snail species, but shrimp extract was also used as a control odor

(to distinguish fondling from feeding response). Phylogeny of the

snails is given. The column labeled "KEY" indicates the symbol for

identification of test odors given on result figures ...... 6

Table 2. Shell occupancy patterns for the seven hermit crab test species

collected in study area. Bold type indicates snail species that

served as sources of test odors in this study ...... 7

V1 List of Figures

Figure 1. Percentage fondling of Clibanarius vittatus in response to snail odors.

Rank shows most commonly occupied shells by C. vittatus. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N=133 for each coupled control/treatment

sequence ...... 12

Figure 2. Percentage fondling of Clibanarius tricolor in response to snail odors.

Rank shows most commonly occupied shells by C. tricolor. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N=147 for each coupled control/treatment

sequence ...... 14

Figure 3. Percentage fondling of Dardanus venosus in response to snail odors.

Rank shows most commonly occupied shells by D. venosus. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N= 131 for each coupled control/treatment

sequence ...... 16

Figure 4. Percentage fondling of Dardanus fucosus in response to snail odors.

Rank shows most commonly occupied shells by D. fucosus. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N=28 for each coupled control/treatment

sequence ...... 18

Figure 5. Percentage fondling of Pagurus pol/icaris in response to snail odors.

Rank shows most commonly occupied shells by P. pollicaris. "*" indi­

cates significant difference between pairwise control and treatment

Vl1 trials for a given snail odor. N=37 for each coupled control/treatment

sequence ...... 20

Figure 6. Percentage fondling of Pagurus Jongicarpus in response to snail odors.

Rank shows most commonly occupied shells by P. Jongicarpus. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N=101 for each coupled control/treatment

sequence ...... 22

Figure 7. Percentage fondling of Pagurus annulipes in response to snail odors.

Rank shows most commonly occupied shells by P. annu/ipes. "*" indi­

cates significant difference between pairwise control and treatment

trials for a given snail odor. N=138 for each coupled control/treatment

sequence ...... 24

VU1 INTRODUCTION

The shells from dead gastropods are important habitat resources for hermit crabs and other organisms in many marine environments (Reese, 1968, 1969; Grant & Ulmer,

1974; McLean, 1974,1975,1983; Young, 1979; Hazlett, 1980, 1981; Abrams, 1980;

Bertness, 1981; Rittschof, 1980a,b; Katz & Rittschof, 1993). Empty shells are utilized by hermit crabs for habitat while the shell surface serves as a substrate for various epifauna such as barnacles, sea anemones and porcellanid crabs (Jensen et al. , 1973; McLean,

1983; Brooks et al. , 1995 ). On the death of the gastropod, the vacated shell becomes available to the hermit crab community (McLean, 1974; Spight, 1977; Herrnkind et al. ,

1981 ; Wilber and Herrnkind, 1982, 1984; Kratt & Rittschof, 1991 ). Because hermit crabs have been only rarely observed searching for and killing live snails to obtain shells

(Brownwell, 1977; Rutherford, 1977 ) only three mechanisms remain: 1) wait until a snail dies or is killed by another predator, 2) obtain shell when a conspecific dies, or 3) exchange shells with other hermit crabs. Shell exchanges between crabs are common

(Hazlett, 1981 ; Katz & Rittschof, 1993) and can involve either negotiation (Hazlett,

1978, 1983) or aggression (Elwood & Neil, 1986) depending on the species of hermit crab.

Obtaining shells directly from dying or dead snails has been demonstrated in only a few species of hermit crabs. In the initial study of chemically-mediated responses by hermit crabs, McLean ( 1974) established "predation sites" in the field where snails were being consumed and observed the subsequent attraction and aggregation of Pagurus pollicaris and P. /ongicarpus at these sites. He concluded that the hermit crabs were attracted to chemical cues from the snails. Subsequently, Rittschof ( 1980a) observed similar behavior by the same two pagurids as well as by the diogenid Clibanarius vittatus.

1 In subsequent studies (Rittschof, 1980b; Kratt et al., 1991 }, the chemical cues were identified as peptides that are produced during proteolytic degradation of the prey snail's muscle. The use of chemical cues to locate shells from a distance is more efficient than actually searching for available shells ( Rittschof, 1980a; Spight, 1985; Katz

& Rittschof, 1993). Once chemical cues bring the hermit crab in contact with the shells, physical features of the shell can be used to make final selection (Reese, 1963;

Bertness, 1980).

Hermit crabs do not enter gastropod shells randomly (Reese, 1962, 1963; McLean,

1974,1975; Grant & Ulmer, 1974;·Conover, 1978; Hazlett, 1981). Snail phylogeny has been shown to influence shell selection by hermit crabs. Specifically, shell architecture and other features related to phylogeny such as weight, internal volume and aperture width are important criteria in shell selection (Reese, 1962, 1963; Conover, 1978, 1979;

Hazlett, 1970; Vance, 1972; Spight, 1985). The importance of snail phylogeny can also be related to chemically-mediated shell acquisition. Some hermit crabs can discriminate odors of different snail species (Rittschof, 1980a). These odors may contain information which the crabs use to correlate physical features specific to the snail species.

Terrestrial hermit crabs in search of shells do not respond to snail odors (even though their larvae are aquatic), but do respond to odors of conspecifics and marine hermit crabs within the intertidal zone (Small & Thacker, 1994; Thacker, 1994).

Shell selection is based partly on actual preferences for certain species of snail and partly on the availability of shells in the habitat (Reese, 1962; Hazlett, 1981 ). Several studies have identified preferences based on shell phylogeny which were specific to local hermit crab populations (Reese, 1962; McLean, 1974; Hazlett, 1980,1981; Hazlett &

Herrnkind, 1980; Rittschof, 1980a). McLean ( 197 4) found that P. pol/icaris was

2 chemically attracted to sites where Fascia/aria hunteria and Polinices duplicatus were the prey species. In the field P. pollicaris typically occupies P. duplicatus (Young, 1979) and F. hunteria shells (Hazlett, 1980). Clibanarius vittatus has responded to chemical cues from dying Melongena corona (Hazlett & Herrnkind, 1980; Rittschof, 1980a,b;

Hazlett, 1982) and Busycon contrarium (Hazlett & Herrnkind, 1980) snails. This finding is in agreement with the natural shell occupancy patterns for C. vittatus (Hazlett &

Herrnkind, 1980; Hazlett, 1980).

There were also snail species that failed to trigger responses by hermit crabs.

Hazlett & Herrnkind ( 1980) found that C. vittatus did not attend sites where F. tulipa or

Thais haemastoma were prey. Rittschof (1980b) found that C. vittatus was not attracted to predation sites of Pleurop/oca gigantea or B. contrarium, and only one of 12 C. vittatus appeared at a F. hunteria predation site.

Rittschof also found that the response of C. vittatus to snail odors was affected by the quality of the crab's shell (Rittschof, 1980a; Hazlett, 1982; Rittschof, et al. , 1992; Katz

& Rittschof, 1993). C. vittatus in poor-fitting shells (Rittschof, 1980a), small-fitting

(Gilchrist & Abele, 1984; Katz & Rittschof, 1993), or fouled shells (Hazlett & Herrnkind,

1980) were more likely to be attracted to snail odor, presumably because an exchange would be beneficial (Rittschof, 1980b; Hazlett, 1983; Katz & Rittschof, 1993). Hermit crabs in poor quality shells respond by investigating or "fondling" nearby shells, using their chelipeds to probe the shell exterior and interior (Rittschof et al. , 1992). Hermit crabs in "suitable" (i.e., properly fitting or unfouled) shells, however, either fled the area or withdrew into their shell. This response may be to avoid wasting time and energy in social interactions which have no benefit and increase the risk of having their shell taken away (Rittschof et al. , 1992).

The present study addressed four questions: 1) Is chemotaxis to snail odors

3 prevalent among hermit crabs? 2) Do members of hermit crab lineages respond similarly to common snail odors? 3) Do hermit crabs respond more acutely to snails whose shells they most frequently occupy? and 4) Does snail phylogeny influence responses by hermit crabs? Representatives from two families of hermit crabs, Diogenidae and Paguridae, were tested. Specifically, two sets of diogenid congeners ( Clibanarius vittatus and C. tricolor, Dardanus venosus and D. fucosus), and three pagurid congeners (Pagurus po/licaris, P. longicarpus, and P. annulipes) were tested. Fifteen species of snails from

11 families served as the test odors. Hermit crab response was measured by the frequency of fondling displays evoked by the odor.

MATERIALS AND METHODS

1. Hermit crab and snail species

C/ibanarius vittatus and C. tricolor were collected locally at North Lake Worth and Bear Cut Preserve, Florida, respectively. Dardanus venosus and D. fucosus were purchased from the Florida Keys Marine Lab in Key West, Florida, where they had been collected in lobster traps at depths> 20m. Pagurus po/licaris and P. longicarpus were collected near the Duke University Marine Laboratory in Beaufort, N.C. Pagurus annulipes was collected at North Lake Worth, Florida. Most hermit crabs were collected from August through September 1995. An additional set of both Dardanus spp. was collected during March 1995. Crab size in carapace width was measured using calipers.

Fifteen species of snails from 11 families served as test odors (see Table 1) .

Snail species were selected based upon their distribution in relation to the hermit crabs and availability. Hermit crabs were tested with odors of sympatric snail species (when the live snail was available) whose shells they also frequently occupied. Additionally,

4 crabs were exposed to odors of snail species not found in their habitat. Specific shell occupancy patterns of each of the seven hermit crabs were determined, by counting the number of shells occupied of each snail species (Table 2). All snails (except for

1/yanassa obsoleta from Beaufort, N.C.) were collected in Florida or purchased from a marine supply company (Gulf Specimen Company) in Panacea, Florida. Shrimp odors were used to distinguish feeding behavior from fondling behavior.

2. Crab maintenance

Prior to testing, hermit crabs were maintained at Gumbo Limbo Marine Laboratory

(GLML) and at the Department of Biological Sciences at Florida Atlantic University.

Crabs at GLML were kept en masse in 380 liter tanks with constantly circulating fresh sea water from the Atlantic Ocean. Crabs at Florida Atlantic University were kept in groups of

5-8 individuals in 18.9 and 37.9 liter aquaria with sea water supplied from GLML. Hermit crabs were tested within 48 hours of collection to allow them time to acclimate to laboratory conditions, but minimize the chances of shell exchanges taking place (that would occur during extended holding periods). Water temperature range in the tanks/aquaria was 22-23°C. Specific gravity of the water was 1.022-1 .025. Hermit crabs were fed flake fish food every other day.

5 Table 1. Odors presented to hermit crabs during bioassays to test for shell-investigative or fondling behavior. Most odors were extracts from snail species, but shrimp extract was also used as a control odor (to distinguish fondling from feeding response) . Phylogeny of the snails is given. The column labeled "KEY" indicates the symbol for identification of test odors given on result figures.

KEY PHYLOGENY

Family Fasciolariidae A1 Fascia/aria hunteria A2 F. tulipa A3 Pleuroploca gigantea Family Melongenidae 81 Me/ongena corona 82 Busycon contrarium 83 B. carica Family Naticidae C Polinices dup/icatus Family Cerithiidae D Cerithium spp. Family Potamididae E Batil/aria minima Family Nassariidae F 1/yanassa obsoleta Family Buccinidae G Cantharus cancellaria Family Muricidae H Murex pomum Family Strombidae Strombus alatus Family Thaididae J Thais haemastoma Family Turbinidae K Turbo castaneus L Shrimp(Penaeus) extract

6 Table 2. Shell occupancy patterns for the seven hermit crab test species collected in study area. Bold type indicates snail species that served as sources of test odors in this study.

------·------

DIOGENIDAE

1. Clibanarius vittatus( n= 133) 2. C. tricolor (n=147) 100% Melongena corona 60% Batillaria minima 40% Cerithium spp.

3. Dardanus venosus (n=131) 4. D. fucosus (n=28) 44% Fascia/aria tulips 42% Fascia/aria tulipa 37% Busycon spiratum 42% Busycon spiratum 5% unidentified snail species 6% unidentified snail species 4% F. hunteria 4% F. hunteria 4% P/europloca gigantea 4% P. duplicatus 4% Polinices duplicatus 2% B. contrarium 1% B. contrarium

PAGURIDAE

5. Pagurus pollicaris (n=37) 6. P. /ongicarpus ( n= 101 ) 7. P. annulipes (n=138) 43% Polinices dup/icatus 1 00% 1/yanassa obsoleta 65% B. minima 19% Busycon carica 26% Cerithium spp. 17% Fascia/aria hunteria 9% unidentified 8% F. tulips 7% B. contrarium 3% B. spiratum 3% unidentified snail species

7 3. Extract preparation and experimental apparatus

Trials were performed at FAU's Gumbo Limbo Marine Laboratory where the holding tanks are equipped with outlets for sea water flow from the Atlantic Ocean. Snail extract was prepared by freezing, then thawing, the flesh to simulate odor release from a predation site. This freeze-thaw method releases endogenous proteolytic enzymes that cause the degradation of proteins into peptide molecules. These molecules mimic the degradation process that occurs when a snail is being preyed upon (Rittschof, 1980b).

One gram of frozen flesh (muscle tissue) from one snail was placed in 5 ml of sea water for 30 min to allow time for the molecules to diffuse in the water. Five milliliters of snail flesh extract were used in each trial, performed in 380 liter tanks. Proportional amounts of snail extract were used for trials done in buckets and trays. The technique was modified after that used by Katz & Rittschof ( 1993 ), where 12 liter buckets were used as artificial tide pools. In my experiments the test arenas were: 19 liter buckets for small hermit crabs, trays (60 x 15 x 33 em) for medium crabs, and 380 liter tanks for large crabs.

4. Experimental procedure

Shell-seeking behavior in response to snail odor can be demonstrated in the laboratory by shell investigation or "fondling" of neighboring crabs ( Rittschof et al ., 1992;

Rittschof, 1980b). Investigative behavior is identified when one crab probes another shell with its chelipeds and first pereiopods. The number of crabs investigating the shells, or

"fondling" neighboring crabs, was recorded.

Groups of conspecific crabs were tested in coupled control and treatment trials. A control was performed prior to each treatment by placing a group of approximately 40 crabs in a tank (with no flow) with 95 liters of sea water. Hermit crabs were added to the test arena (either a bucket, tray, or tank) and the water stirred by hand (this was to

8 control for the stirring that was done in odor trials). Once the water settled (usually 10-15 sec), the number of crabs fondling was recorded during the next 2 min. No crab was counted more than once in any trial.

Immediately following the control observations (i.e., the first 2 min. period), the odor presentation was performed on the same group of crabs (which remained in the same arena) by adding 5 ml of snail flesh extract with a syringe to an area directly below which there were no crabs. Again, the water containing the crabs was stirred, this time to mix the odor molecules. After the water settled, the number of fondling crabs was recorded for an additional 2 min. Thus, the paired control and treatment for each group of crabs was done in approximately '5 min. The first group of conspecifics was then removed from the arena and remaining individuals were tested in similar-sized groups until all had been tested with the specified odor.

At this point, the arena was drained, rinsed and refilled with fresh sea water for additional trials with individuals of the same crab species for the remaining snail odors.

To control for possible sequence effects, presentation of the different snail odors was randomized for each hermit crab species. All snail odors were presented in one overall session (about two hours total) to minimize shelf exchanges between trials.

Large hermit crabs, such as Dardanus venosus (14.1-16.0 mm carapace width), were tested in 380 liter tanks. To keep group sizes and relative area similar to the larger crab group, small crab species (0.5-2.7 mm carapace width), such as C. tricolor, and medium-sized crab species (4.5-5.2 mm), such asP. pollicaris, were tested in 19 liter buckets with 4 liters of water or trays with 9.5 liters of water, respectively. Proportional amounts of snail extract were used for trials done in buckets and trays.

Katz & Rittschof (1993) and Brooks et al, (1995) showed that clipping the shelf to reduce its size may increase fondling behavior of hermit crabs. This is an invasive

9 procedure, however, which involves extensive handling and possible injury to the crab

(especially small species) and may not reflect the natural responses of crabs in the field.

Thus, I chose to test animals initially, as collected, in unaltered shells. If a hermit crab species proved to have little fondling activity (in both control and treatments) and individuals were large enough to handle quickly and safely, then clipping of shells was performed and individuals isolated between all trials (to prevent moving out of their

"small" shells).

Totals from the control and treatment groups were converted to percentages.

Differences between the control and treatment groups were analyzed by the proportion test (z test), using a p .s 0.05 criterion for significance.

RESULTS

Diogenids

Clibanarius vittatus (Fig. 1) displayed significant increases in fondling behavior compared to controls in response to odors from Melongena corona (z = 2.73, p = 0.006) and Polinices duplicatus (z=2.29, p=0.021 ). M. corona was the only shell occupied by C. vittatus in my samples.

C. tricolor (Fig. 2) displayed significant increases in fondling behavior compared to controls in response to odors from Fasciolaria tulipa (z = 2.64, p = 0.008) and F. hunteria, (z = 2.33, p = 0.019), Pleuroploca gigantea (z = 2. 78 , p = 0.005) and P. duplicatus (z = 2.50, p = 0.012). Cerithium spp., which was one of the most frequently occupied shells by C. tricolor, failed to elicit a significant increase in fondling behavior.

Two different sets of Dardanus venosus crabs were tested; one set collected during March 1995 and the second set during September 1995. The first set of crabs displayed almost no fondling behavior (in controls or treatments), even in subsequent

10 tests in which their shells were clipped back. The second set of crabs (in unaltered shells) collected during the fall, however, showed significant increases in fondling behavior (without clipping) compared to controls in response to odors from B. carica (z =

2.20, p = 0.028), shrimp extract (z = 2.71 , p = 0.007), F. tulipa (z = 2.20, p = 0.028) and

C. cancellaria (z =2 .20, p = 0.028) (Fig. 3). F. tulipa was the most frequently occupied shell by D. venosus (44%), but it was also found in shells of F. hunteria. No crabs in my samples were found in C. cancellaria (Table 1).

Two different sets of D. fucosus were also collected simultaneously to those of

D. venosus, with similar results. The spring-collected crabs were inactive (even after shell clipping), but the fall-collected crabs showed significant increases in fondling behavior compared to controls in response to B. carica (z =2 .13, p = 0.033), shrimp extract (z = 2.42, p = 0.015) and S. a/atus (z = 2.70, p = O.OO?)(Fig. 4). Busycon contrarium, Fasciolaria hunteria, F. tulipa, and Polinices duplicatus were the most frequently occupied shells by D. fucosus. No crabs in my samples occupied shells of S. alatus (Table 1 ).

Pagurids

Even though an apparent trend of increased activity by the pagurids (Figs. 5-7) occurred, treatment responses were not statistically different from their controls.

Subsequent attempts to increase motivation of P. pol/icaris individuals by clipping the shells produced no changes in response.

11 Figure 1. Percentage fondling of Clibanarius vittatus in response to snail odors. Rank shows most commonly occupied shells by C. vittatus. "*" indicates significant difference between pairwise control and treatment trials for a given snail odor. N=133 for each coupled control/treatment sequence.

12 Clibanarius vittatus

K ,.,... ,.,.,.,.,.,.,.,.,.,.,.,.,. [l] Control §] Treatment

I :-:·:·:·:-:-:-:-:-:-:-:-:-:-:-:-:-:·:·:·:·:·:·:·:·:·:·:·:·:·:·:·:·:·

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81 ;.;.;.;.;.;.;.;.;.;.; .;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;.;. * ( 1 ) A3 ·:·:···:·······:·:·:·:·:·:·······:·····:···:·:·····:·:·:·:·:·:·:·:·:·:·:·:·:·:·:···:·:

A1 ,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.,.

0 2 4 6 8 10 12 14 16 %FONDUNG

13 Figure 2. Percentage fondling of Clibanarius tricolor in response to snail odors. Rank shows most commonly occupied shells by C. tricolor. "*" indicates significant difference between pairwise control and treatment trials for a given snail odor. N=147 for each coupled control/treatment sequence.

14 Cllbanarlus tricolor [ill Control Treatment K ~ [ffij

J -~~!lll!!lllmllllllmlml!lllmll , ~ H ,.,.,.,.,.,., ... ,., .....,., .. ., ...... ,., ......

B2 .ii. ili,., ... ,.,.ili.... ,., ...a ····· .. llllllll1l!il!l~~~ 81 ·.··.··· · ······ ·····.· P-3 = * /42. ·················:·····:···········:·····:·········· * A1 = * 0 2 4 6 8 10 o/o FONDLING

15 Figure 3. Percentage fondling of Dardanus venosus in response to snail odors. Rank shows most commonly occupied shells by 0. venosus. "*" indicates significant difference between pairwise control and treatment trials for a given snail odor. N=131 for each coupled control/treatment sequence.

16 Dardanus venosus

L imlmllrnllmllrnlmmi"

H --~·BTI:-:-:-:-:-:m:J-:·:·:·:·

~ G iml!mll!iil!if.!.m'llli~:mliilll!l!if.!.m'llliirlif:lmll!if.!.m'lllimmi!lliif.!m~Emml * @ 35 c ~-:ii.,.,.,.,ii.,.,.,.,w·:·:-w:- : -:-:-p:·:<·:-:§]-:-:-: -:§]- : -:-: -:-§:-:-:-:-m::;]:-:-:-:- ( 4 J

....1 ~~ ~~~~~~~~~~ * B2 -fj'''''@j'''''''"'@j''''''''''ij·:·:·:-:-:-ii: · : ·:-~:-:-:·:·:·:£]·:·:·:·:·:£]·:·:·:·:·:6· ~:ml ( 5 J

81 ·-m;:-:-: -~:·:·:·: · :·ljj: · :.>:·:m;·:·:·:·:·ifj: · :·:·:·: A3 :-:-:-:-:-:-: .;.;.;.;.;.;.:-:-:-:-:·:·:·:-:-:-:·:·:·:·:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-: ( 4 J

A2. ~mmil!if.!.m'lllimmi:mliilll!l!if.!.m'llliirlifllmll!if.!.m'lllimmi!lliif.!ml!if.!.m'llli:mliilll!l * ( 1 J A1 ~~-::~:::: ~· ~~~~(i4 ~) ------0 2 3 4 5 6 7 %FONDUNG

17 Figure 4. Percentage fondling of Dardanus fucosus in response to snail odors. Rank shows most commonly occupied shells by D. fucosus. "*" indicates significant difference between pairwise control and treatment trials for a given snail odor. N=28 for each coupled control/treatment sequence.

18 Danlanus fucosus Limmmmmmmmmmmmmmmmmmmmmmmmmmmmmm* BJ Control illfi Treatment K ~mmmmmmmmmmmmmm

J ·.•.•.y.•,•,•,,,.,., ••,.,.,,•,•,• * H-

81 - ft:3 imJmm:;1!mmlmmm!!im!~m!!im!~mmmm!l A2 .iij'''''''iij''''·'''''!b' ~ { 1 )

A1 ~~~~J(~3i) ______0 5 10 15 20 25 30 o/oFONDUNG

19 Figure 5. Percentage fondling of Pagurus pollicaris in response to snail odors. Rank shows most commonly occupied shells by P. pollicaris. "*" indicates significant ddifference between pairwise control and treatment trials for a given snail odor. N=37 for each coupled control/treatment sequence.

20 Pagurus poll/earls l£l Control miJ Treatment K -

H- C/) !!! G () w 3; c ( 1 J ...J ~B3 ( 2 J C/) 82 - ( 5 J 81

/43

A2

A1 ( 3 J 0 1 2 3 4 5 6 7 8 %FONDUNG

21 Figure 6. Percentage fondling of Pagurus longicarpus in response to snail odors. Rank shows most commonly occupied shells by P. longicarpus. "*" indicates significant difference between pairwise control and treatment trials for a given snail odor. N=1 01 for each coupled control/treatment sequence.

22 Pagurus longicarpus 0] COntrol

K ·······:·:···································=-········:·········:························· im) Treatment

J , , ,•,,N,,,•,,,,,,,•,,•,•,•,,,•,,,•,,•,•,,,,,w,

..:-:- .·:-:-:-:-:-:-:-:·:·:·:·:-:-:·:·:·:·:·:·:·:·:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-:-;.;.;.;.;.;.;.;.;.;.;-:-:-:-:-:-:-:-:-:-:-: H ...... f3 G ·=·=·=·=·=·=· .. =·=·=·=·=·=·=·=·=·=·=·=·=·=·.

~ F '•'•'•:•'•'•'•'•'•:·····:•:•'•'•'•'•'•'•'•'•'•'•'•'•'•'•:•'•'•'•'•'•'•'•'•'•:•:···:•'•'•'•'•'•'•'•'"'•:.;.;.•.;.·.•.·,•.w.;.·.·. .,. ( 1 ) ...J c ..... ·.•.·.·,•.•,•.•,•,•,•,•,•,•,•,·,·,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,•,

~ B3 ··=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=·=''·=·=·=·=·=·=·=·=···=···:·:···:.'·:·:·:·:·:·: ·=·=·='···:·:·:···=·=·=·=·=·>:·:·:

B2 iemllillllll!lllllllillllll!lllllllillllll!lllllllillllll!lllllll!illll e1 ~~~.. d ... ~.. d...... d...... a ...... a.....m .. ~... m .. ~.... d ...... d. ~~~~~ /4:3 .·.·.··:·········:· A2 ,,,.,,,,,,,...

0 1 2 3 4 5 6 %FONDLING

23 Figure 7. Percentage fondling of Pagurus annulipes in response to snail odors. Rank shows most commonly occupied shells by P. annulipes. 11 *11 indicates significant difference between pairwise control and treatment trials for a given snail odor. N=138 for each coupled control/treatment sequence.

24 Pagurus annulipes

[ill Control

K ········:·:·:-'·:·:···:·:···=·=·······=·=·····:·:···=·=·=·=·=·=···=·=·=·=·=···=·=·=·=····· 111m Treatment

H ...... ·.·.····. ·· ·.····

~ G 4=m=-=· m···=··e··,· m··=·=·=m·-·:-:- e,·e=·=·=·= e=-=·'&':-:-·m·=···m>:···m"·m=·=·=·=·m=·.···m,···~·,··~···=·~=·=· ~=:-:-~:-:-·=~··=·· ~= · =··=m·=·=·=· bm~~ frl E =·····=·········:·······=···:·······=·····=···············:·Y·····=·=·········=···=···=··········· ············································ ·.·.·.·.·.·.·.·.· ..... ·.·.·.·.·.·.·.··································· ( 1 ) ~ c ~-.·~~········'·iij····ii" ijl· ~~ ~~~~~~-- 82 .;.;.;.;.; .;.;.;.;.;.-.;.;.;.-.·. ·······'·'< ·:·:·:·:·:·:'·:·:

B1 =·=·=·=·=·=·=·=·=·=·=·=·=·=•·=·=·=·=·=·=···

P-3 -,mllllrml'l!llllrml'l!llllrml'l!~~~~~ Kl ilmiiiiiiii~~-lllli!lll!lllll A1 ··························· 0 1 2 3 4 5 6 %FONDLING

25 DISCUSSION

Prevalence of Responses

In the present study, shell investigative behavior or fondling was seen in all seven species of hermit crabs. Only members of the Diogenidae, however, displayed significantly increased investigative behavior in response to snail odors. Specifically,

Clibanarius vittatus, C. tricolor, Dardanus venosus, and D. fucosus fondled in response to various snail odors. C. vittatus and D. venosus have been observed previously either attending predation sites in the field or fondling (Hazlett and Herrnkind, 1980; Rittschof,

1980a; Rittschof et al. , 1992; Brooks et al. , 1995 ). Thus, their positive response to snail odors in my study are consistent with previous works. C. tricolor and D. fucosus, however, had not been previously shown to investigate shells in response to chemicals released from snail muscle. Members of the Paguridae showed limited responses to snail odors in this study. Differences in responses among and between these two families of hermit crabs may be related to complex interactions of both physical and biotic factors (including genetic differences related to phylogeny), as well as experimental procedure.

The local habitat in which the crabs are located may influence how crabs respond to chemical cues. For example, C. vittatus used in this study inhabited a relatively "calm, clear'' mud flat environment (North Lake Worth), which might facilitate the detection of and migration to gastropod chemical signals. Thus, these crabs may be attuned to high response levels. C. tricolor also inhabits a relatively calm area (Bear Cut

Preserve, Florida). Individuals of C. tricolor were very active fondlers, responding to 4 of the 15 odors despite being in well-fitting shells.

Another possible explanation for the significant investigative behavior by C.

26 vittatus is shell availability. There were few suitable empty shells in the North Lake Worth area where C. vittatus was collected; this situation can trigger increased fondling behavior (Rittschof, 1980a; Hazlett and Herrnkind, 1980). P. longicarpus used in this study were found in areas with an abundance of //yanassa obso/eta (which most crabs also occupied), which may mean this population of crabs relies less on chemically­ mediated shell acquisition. C. tricolor, however, inhabits an area (Bear Cut Preserve,

Florida) also with an abundance of shells, Batil/aria minima (which most crabs occupied), but yet still responded keenly to snail odors. This apparent enigma illustrates the difficulty to ascribing single factors as triggers for these complex behaviors.

The results for the Oardanus spp. further illustrate the complexity of these responses. Individuals of both species tested in the spring showed little activity, even after clipping the shells to "motivate" them to fondle. Individuals collected and tested in the fall of the same year, however, showed both high baseline levels and increased fondling activity to certain snail odors. Even though the Oardanus spp. collected for this study are subtropical, seasonal changes in the fall may stimulate individuals to find new

(and perhaps larger) shells possibly as preparation for subsequent, extended periods of low shell availability.

The fall-collected 0 . venosus responded significantly to 4 out of 13 odors and 0 . fucosus to 3 out of 13 odors. One odor in each of the sets of stimulatory odors for both crabs, however, was shrimp extract. This response to a non-gastropod odor was surprising because several studies by Rittschof indicate that hermit crabs do not fondle in response to chemical cues from food sources or from flesh sources such as crustacean or bivalve muscle ( Rittschof, 1980a; Rittschof et al. , 1990; Rittschof et al. , 1992; Katz and

Rittschof, 1993). Furthermore, hermit crabs were tested within 48 hours of capture and, thus, should not have been hungry. Similarity in peptide sizes or sequences in shrimp

27 and gastropod odors to which Dardanus spp. respond might explain these results.

Shrimp odors might also contain cues similar to the blood cues of conspecific crab odors, which are also known to elicit investigative responses in some hermit crab species

(Rittschof et al. , 1992).

The relatively low levels of fondling behavior (compared to the diogenids) by the three Pagurus spp. crabs was surprising, because both P. pollicaris and P. longicarpus have been observed attending predation sites (Mclean, 1974; Rittschof et al. , 1992). An explanation for the differences may be related to genetic and behavioral differences unrelated to the ability of the crabs to discriminate odors. The pagurids often seemed less aggressive and active than the diogenids. Often, individuals remained motionless for periods of time (see Hazlett, 1979). This inactivity was especially noticeable for P. pollicaris. Additionally, Rittschof (1980a) noted that P. pollicaris was less likely than C. vittatus to migrate to a predation site. Attempts to stimulate increased fondling behavior by clipping the shells proved ineffective for P. pol/icaris. Thus, the behavioral assay used in my study may be more conducive for the more generally active diogenids.

Patterns of Responses within Hermit Crab Lineages

Some patterns of responses to snail odors were present among congenerics.

Both Clibanarius spp. showed increased fondling in response to Polinices duplicatus, which is not a snail I found inhabiting the areas where the crabs were collected.

Additionally, C. tricolor used in this study were incapable of inhabiting the P. dup/icatus because the shells were too large. Both Dardanus spp. showed significantly increased fondling in response to Busycon carica, which is closely related to a common shell (B. spiratum) in the area inhabited by both species. The Dardanus spp. also responded significantly to shrimp odor, which (as previously discussed) may indicate similarity of molecules in shrimp and gastropod and/or conspecific odor.

28 Patterns in responses by the pagurids were difficult to determine, because of relatively low levels of fondling activity. P. /ongicarpus and P. annulipes, however, did appear to have higher baseline activity levels than P. pol/icaris.

Shell Occupancy Patterns and Responses

As hermit crabs grow and increase in size, their preference for gastropod shells can change (Reese, 1962). This occurs because larger, older hermit crabs must occupy an array of larger shells which are usually of a different species and lower availability than the smaller ones previously utilized (Reese, 1962, 1963; Fotheringham, 1976a,b;

Rittschof, 1980b; Wilber & Herrnkind, 1982). Thus, specific patterns increasing the likelihood of locating and occupying these shells should evolve.

Two crab species in this study, C. vittatus and D. venosus, showed this predicted pattern by responding significantly to odors of snails whose shells they frequently occupy.

C. vittatus increased fondling behavior in response to Me/ongena corona. All of C. vittatus collected in this study area (North Lake Worth) were found occupying M corona shells (see Table 2). Previous studies have shown that C. vittatus selectively responds to odors from M corona in the field (Hazlett and Herrnkind, 1980; Hazlett 1980, 1982;

Rittschof, 1980a,b) and appears to be the preferred shell species of this crab in many environments (Brooks & Mariscal, 1985). It would be of interest to determine the plasticity of this response by changing the shell species occupied by C. vittatus and seeing whether its response to M corona odors diminished. Additionally, would C. vittatus individuals of populations found predominantly in other shell species have patterns of response specific to their different shells?

D. venosus also showed responses correlated to shell occupancy, responding to

Fasciolaria tulipa. This was the predominantly occupied shell for this crab in the study area (see Table 2). Again, this response should increase the chances of D. venosus

29 locating and occupying this shell. Interestingly, although 0 . fucosus has similar shell occupancy patterns to D. venosus, the former crab had a very low response to F. tu/ipa.

This indicates differences do exist, as is predicted (i.e., competitive exclusion theory), between these two closely-related, sympatric species.

Snail Phylogeny and Responses

Lastly, I tried to determine if there was a correlation between responses by hermit crabs and phylogeny of snails. Specifically, similarities in responses to closely related snail species such as Melongena corona, Busycon contrarium, and B. carica (all of which belong to the Family Melongenidae) might occur because chemical signals among confamilials may be more similar than between snail families. C. vittatus responded significantly to Melongena corona but to neither Busycon spp. Whereas, both Dardanus spp. responded to Busycon carica, but neither B. contrarium or Melongena corona were able to elicit a response. Morphologically, B. carica and B. contrarium are the most similar of the three species, which might indicate that hermit crabs would have similar responses to both. To that end, it might also be expected that P. pol/icaris would respond to three closely related species (B. carica, B. contrarium and B. spiratum) found living in the same habitat, especially because these shells are commonly used by this species

(Steve Schenk, pers. comm.). However, P. pollicaris did not respond to any significantly, thus, no patterns could be determined. B. spiratum was unavailable as a test odor in the present study, but the remaining two Busycon species failed to elicit a response by P. pol/icaris.

C. tricolor responded significantly to all the test odors from the Family

Fasciolariidae: Fasciolaria hunteria, F. tulipa and Pleuroploca gigantea. C. tricolor, however, is incapable of utilizing any of these shell species because of extreme differences in size between it and the shell. C. tricolor inhabits an area where there is an

30 abundance of B. minima and Cerithium sp. shells, but did not respond to them. Because of the abundance of these shells, C. tricolor may not depend on chemically-mediated acquisition behaviors to obtain shells. The results of this study indicate that C. tricolor is capable of responding to some snail odors, but may not be capable of discriminating odors as well as other crab species that depend on this mechanism for shells.

Conclusions

In the present study I have expanded the list of hermit crab species that show chemically-mediated behavior in response to gastropod odors, thus, indicating the prevalence of this phenomenon among hermit crab lineages. Additionally, correlations in some cases were made between responses by hermit crabs and 1) other hermit crab lineages, 2) natural shell occupancy patterns, and 3) phylogeny of snails. Further studies are necessary to gain a complete understanding of the mechanisms used by hermit crabs for shell acquisition. Specifically, studies should address the influence of seasonal differences on shell seeking behaviors, as shell availability may vary seasonally. Future studies may reveal other trends or factors related to context, such as reproductive state, that affect or contribute to chemically-mediated responses in hermit crabs.

The mechanisms hermit crabs use to select shells are of evolutionary significance. In areas of intense predation and limited resource availability, chemically-mediated shell selection behavior has evolved in some species to increase search efficiency. The gastropod shell has a vital role in this process and also has a role in the life histories of many other organisms that simultaneously use the shell. In many soft-bottom communities, snail shells represent rare hard substrata. This scarcity makes gastropod shells a key species in many habitats. Therefore, there is a significant relationship between gastropod shells, organisms that use them, and their environment.

31 REFERENCES

Abrams, P.A. , 1980. Resource partitioning and interspecific competition in a tropical hermit crab community. Oecologia 46: 365-379.

Bertness, M.D., 1980. Shell preference and utilization patterns in littoral hermit crabs of the Bay of Panama. J. Exp. Mar. Bioi. Ecol. 48: 1-16.

Bertness, M.D., 1981 . Conflicting advantages in resource utilization: The hermit crab housing dilemma. Amer.Nat. 118: 432-437.

Bertness, M.D. , 1982. Shell utilization, predation pressure, and thermal stress in Panamanian hermit crabs: an interoceanic comparison. J. Exp. Mar. Bioi.Ecol. 64: 159-187.

Brooks, W .R. , L. Ceperley, & D. Rittschof, 1995. Disturbance and reattachment behavior of sea anemones Calliactis tricolor (Le Sueur): Temporal, textural and chemical mediation. J. Chern. Ecol. 21(1): 1-12.

Brooks, W .R. & R.N. Mariscal, 1985. Shell entry and shell selection of hydroid­ colonized shells by three species of hermit crabs from the northern Gulf of Mexico. Bioi.Bull. 168:1-17.

Brownwell, W .N. , 1977. Reproduction, laboratory culture and growth of Strombus gigas, S. costatus, and S. pugi/us in Los Rogues, Venezuela. Bull. Marine Science 27: 668-680.

Conover, M.R. , 1978. The importance of various shell characteristics to the shell selection behavior of hermit crabs. J. Exp. Mar. Bioi. Ecol. 32: 131 -142.

Conover, M.R. , 1979. Effect of gastropod shell characteristics and hermit crabs on shell epifuana. J. Exp. Mar. Bioi. Ecol. 40: 81-94.

Elwood, R.W. & S. Neil, 1986. Asymmetric contests involving two resources. J.Theor.Biol. 120: 237-249.

Fotheringham, N., 1976a. Hermit crab shells as a limiting resource (Decapoda, Paguridea). Crustaceana 31(2): 193-199.

Fotheringham, N., 1976b. Population consequences of shell utilization by hermit crab. Ecology 57: 570-578.

Gilchrist, S. & L.G. Abele, 1984. Effects of sampling method on the estimation of population parameters in hermit crabs. J. Crust. Bioi. 4: 645-54.

Grant, C. & K. M. Ulmer, 1974. Shell selection and aggressive behavior in two sympatric species of hermit crabs. Bioi. Bull. 146: 32-43.

32 Hazlett, B.A., 1970. Tactile stimuli in the social behavior of Pagurus bernhardus (Decapoda, Paguridea). Behaviour 36: 20-48.

Hazlett, B.A. , 1978. Shell exchanges in hermit crabs: Aggression, negotiations, or both? Anim. Behav. 26: 1278-1279.

Hazlett, B.A., 1979. Individual distance in crustacea: IV. Distance and dominance hierarchies in Pagurus pollicaris. Mar. Behav.Physiol. 6: 225-242.

Hazlett, B.A. , 1980. Communication and mutual resource exchange in north Florida hermit crabs. Behav. Ecoi.Sociobiol. 6: 177-184.

Hazlett, B.A., 1981. The behavioral ecology of hermit crabs. Ann. Rev. Ecol. Syst. 12: 1-22.

Hazlett, B.A. , 1982. Chemical induction of visual orientation in the hermit crab Clibanarius vittatus. Anim. Behav. 30: 1259-1260.

Hazlett, B.A. , 1983. Interspecific negotiations: Mutual gain in the exchanges of a limiting resource. Anim. Behav. 31: 160-163.

Hazlett, B.A. & W . Herrnkind, 1980. Orientation to shell events by the hermit crab Clibanarius vittatus (Bose) (Decapoda, Paguridae). Crustaceans 89: 311-314.

Herrnkind, W., P. Wilber, and J. Loftin, 1981 . Shells traveling from snails to hermit crabs: A rapid transit system? Am. Zool. 21(4): 991.

Jensen, K. & K. Bender, 1973. Invertebrates associated with snail shells inhabited by Pagurus bernhardus (L.) (Decapoda). Ophelia 10: 185-192.

Katz, J.N. & D. Rittschof, 1993. Alarm/investigation responses of hermit crabs as related to shell fit and crab size. Mar.Behav. Physiol. 22: 171-182.

Kratt, C.M. & D. Rittschof, 1991 . Peptide attraction of hermit crabs Clibanarius vittatus Bose: Roles of enzymes and substrates. J. Chem.Ecol. 17: 2347-2365.

Mclean, R.B. , 1974. Direct shell acquisition by hermit crabs from gastropods. Experientia 30: 206-208.

Mclean, R.B., 1975. A description of a marine benthic faunal habitat web. PhD Dissertation, Florida State University.

Mclean, R.B., 1983. Gastropod shells: a dynamic resource that helps shape benthic community structure. J. Exp. Mar. Bioi. Ecol. 69: 151-174.

Reese, E.S., 1962. Shell selection behavior of hermit crabs. Anim. Behav. 10(3/4): 347-360.

Reese, E.S., 1963. The behavioral mechanisms underlying shell selection by hermit crabs. Anim. Behav. 10: 347-360.

33 Reese, E.S., 1968. Shell use: An adaptation for emigration from the sea by the coconut crab. Science 161 : 385-386.

Reese, E.S., 1969. Behavioral adaptations of intertidal hermit crabs. Am. Zool. 9: 343-355.

Rittschof, D., 1980a. Chemical attraction of hermit crabs and other attendants to gastropod predation sites. J. Chern. Ecol. 6: 103-118.

Rittschof, D., 1980b. Enzymatic production of small molecules attracting hermit crabs to simulated gastropod predation sites. J. Chern. Ecol. 6: 665-675.

Rittschof, D., C.M. Kratt, & A.S. Clare, 1990. Gastropod predation sites: the role of predator and prey in chemical attraction of the hermit crab C/ibanarius vittatus ...J. Mar. Bioi. Ass. U.K. 70: 583-596.

Rittschof, D., D.W . Tsai, P.G. Massey, L. Blanco, J.L. Kueber, Jr. and R.J . Haas, Jr., 1992. Chemical mediation of behavior in hermit crabs: alarm and aggregation cues. J. Chern. Ecol. 18: '959-984.

Rutherford, J.C., 1977. Removal of living snails from their shells by a hermit crab. Veliger 19: 438-439.

Small, M.P., R.W. Thacker, 1994. Land hermit crabs use odors of dead conspecifics to locate shells. Journal of Experimental Marine Biology and Ecology 182: 169-182.

Spight, T.M., 1977. Availability and use of shells by intertidal hermit crabs. Bioi.Bull.152:120-133.

Spight, T.M ., 1985. Why small hermit crabs have large shells. Res. Popul. Ecol. 27: 39-54.

Thacker, W .R. , 1994. Volatile shell-investigation clues of land hermit crabs: Effect of shell fit, detection of cues from other hermit crab species, and cue isolation. Journal of Chemical Ecology 20(7): 1457-1482.

Vance, R.R. , 1972. The role of shell adequacy in behavioral interactions involving hermit crabs. Ecology 53: 1075-1083.

Wilber, T.P., Jr. & W.F. Herrnkind, 1982. Rate of new shell acquisition by hermit crabs in a salt marsh habitat. J. Crus. Bioi. 2(4): 588-592.

Wilber, T.P., Jr. & W .F. Herrnkind, 1984. Predaceous gastropods regulate new shell supply to salt marsh hermit crabs. Mar. Bioi. 79: 145-150.

Young, A.M ., 1979. Differential utilization of gastropod shells by three hermit crab species in North Inlet, South Carolina, U.S.A. Crustaceana 5: 101-104.

34