A Novel Interaction: the Thin Stripe Hermit Crab, Clibanarius

Home , Clibanarius, Clibanarius erythropus, Clibanarius tricolor, Diogenidae, Hermit crab, Lettered olive

A NOVEL INTERACTION: THE THIN STRIPE HERMIT CRAB, CLIBANARIUS

VITTATUS, KILLS THE FLORIDA CROWN CONCH, MELONGENA

CORONA, FOR ITS SHELL

Jennifer Cutter

A Thesis Submitted to the Faculty of

Charles E. Schmidt College of Science

In Partial Fulfillment of the Requirements for the Degree of

Master of Science

Florida Atlantic University

Boca Raton, FL

August 2017 Copyright by Jennifer Cutter 2017

ACKNOWLEDGEMENTS

I would like to thank Florida Atlantic University, Harbor Branch

Oceanographic Institute, and Dr. Donna Devlin for giving me the opportunity to conduct this fascinating study. I would also like to thank the other committee members (Dr. Vincent Encomio, Dr. Edward Proffitt, and Dr. William Brooks) for their help, advice, and guidance. This work was made possible through funding from the Indian River Lagoon Research Fellowship awarded by the Harbor

Branch Foundation and a scholarship awarded by The Broward Shell Club.

Additionally, I would like to thank Dr. Richard Turner for being willing to meet with me on several occasions to answer questions and share his vast knowledge.

iv ABSTRACT

Author: Jennifer Cutter

Title: A Novel Interaction: The thin stripe hermit Crab, Clibanarius vittatus, kills the Florida crown conch, Melongena corona, for its shell

Institution: Florida Atlantic University

Thesis Advisor: Dr. Donna Devlin

Degree: Master of Science

Year: 2017

The hermit crab Clibanarius vittatus kills Melongena corona solely to acquire a better fitting shell. This finding is contrary to previous studies, which found that hermit crabs of other species cannot kill gastropods or, in most instances, remove freshly dead gastropods from their shells. This interaction cannot be classified as predation because Melongena tissue was never consumed. Clibanarius killed Melongena only when by doing so they could trade up to a better fitting shell. It cannot be classified as competition because there is no opportunity for Melongena to gain from the interaction. Therefore the term

“lethal eviction” is hereby proposed for this interaction. The ability to kill a gastropod to obtain a superior shell gives Clibanarius vittatus an evolutionary advantage over other hermit crab species. It is not known if the outcome of this interaction is widespread where both species occur or if it is confined to the study area. v DEDICATION

This manuscript is dedicated to my parents for always encouraging and believing in me. When a girl who lived 400 miles away from the ocean said she wanted to become a marine biologist, you did everything you could to help me realize that goal. You’ve made it possible for me to come this far, and I know you’ll whole heartedly support whatever I choose to do next. I can’t wait to share my future achievements with you.

A NOVEL INTERACTION: THE THIN STRIPE HERMIT CRAB, CLIBANARIUS

VITTATUS, KILLS THE FLORIDA CROWN CONCH, MELONGENA CORONA,

FOR ITS SHELL

LIST OF FIGURES ...... ix

LIST OF TABLES ...... xi

1. INTRODUCTION ...... 1

1.1. Evolutionary and Ecological Significance ...... 2

1.2. Clibanarius vittatus and Melongena corona ...... 6

1.3. Objectives and Hypotheses ...... 8

1.3.1. Manipulative Lab Experiment ...... 8

1.3.2. Manipulative Field Experiment ...... 9

1.3.3. Field Surveys ...... 9

2. MATERIALS AND METHODS ...... 10

2.1. Study Species and Locations ...... 10

2.2. General Experimental Protocol ...... 12

2.3. Manipulative Lab Experiment: Drivers of Shell Acquisition ...... 13

2.4. Manipulative Field Experiment: Interactions between Melongena

andClibanarius vary based on Population Density ...... 18

2.5. Field Surveys: Effect of habitat on population densities and sizes of

Clibanarius and Melongena...... 23

vii 3. RESULTS ...... 27

3.1. Manipulative Lab Experiment: Drivers of Shell Acquisition ...... 27

3.2. Manipulative Field Experiment: Interactions between Melongena and

Clibanarius vary based on population density ...... 31

3.3. Field Surveys: Effect of habitat on population densities and sizes of

Clibanarius and Melongena...... 33

4. DISCUSSION ...... 40

4.1. Drivers of Shell Acquisition ...... 41

4.2. Interactions between Melongena and Clibanarius vary based on

population density...... 45

4.3. Effect of habitat on population densities and sizes of Clibanarius and

Melongena ...... 47

4.4. Ecological Classification of the Interaction ...... 49

4.5. Future Work ...... 49

REFERENCES ...... 51

viii LIST OF FIGURES

Figure 1: Map of study locations...... 12

Figure 2: Containers for manipulative lab experiment ...... 14

Figure 3: Arrangement of treatment groups for manipulative lab experiment .... 14

Figure 4: Comparison of male and female Clibanarius vittatus...... 17

Figure 5: Placement and arrangement of enclosures for the manipulative field

experiment ...... 19

Figure 6: Enclosure utilized for the manipulative field experiment ...... 20

Figure 7: Arrangement of enclosures for the manipulative field experiment ...... 21

Figure 8: Clibanarius vittatus gathered around an enclosure...... 22

Figure 9: Shoreline habitats chosen for surveys ...... 24

Figure 10: Sex of Clibanarius that killed Melongena ...... 28

Figure 11: Shell fit of Clibanarius that killed Melongena ...... 28

Figure 12: Melongena mortality by treament ...... 29

Figure 13: Clibanarius and Melongena with shell aperatures alligned ...... 30

Figure 14: Clibanarius and Melongena simultaneously inside the shell ...... 30

Figure 15: Intact Melongena carcass ...... 30

Figure 16: Clibanarius attraction ...... 32

Figure 17: Melongena survival...... 33

Figure 18: Shell occupants by survey site ...... 35

Figure 19: Shell species by survey site ...... 35 ix Figure 20: Clibanarius shell fit and type ...... 37

Figure 21: Shell length and site ...... 38

Figure 22: Shell length and shell species ...... 39

x LIST OF TABLES

Table 1: Assignation of Clibanarius shell fit ...... 14

Table 2: Primariy survival analyses for the manipulative lab experiment ...... 18

Table 3: Secondary survival analyses for the manipulative lab experiment ...... 18

Table 4: Treatments for the manipulative lab experiment ...... 21

Table 5: Results from survival analyses for the manipulative lab experiment ..... 28

Table 6: Results from MANOVAs for the manipulative field experiment ...... 32

Table 7: Results from Pearson Chi-square test for field surveys ...... 34

Table 8: Abbreviations utilized for snail and shell species ...... 36

Table 9: Results from ANOVA for field surveys ...... 38

xi 1. INTRODUCTION

Hermit crabs are soft bodied crustaceans that utilize shells for protection.

They do not have the ability to produce a shell and thus must obtain it from an external source (Hazlett 1996a, 1996b, Rittschof et al. 1995, Tricarico et al.

2009). While hermit crabs have a suite of behaviors that allow for the acquisition of an optimal shell, previous literature indicates that hermit crabs cannot kill gastropods to directly obtain this resource (Fotheringham, 1976; Bertness 1981b,

Tricarico & Gherardi, 2006; Tricarico et al., 2009; Laidre, 2011). Fotheringham

(1976) stated that hermit crabs “are dependent upon a shell resource…which they apparently cannot obtain from the manufacturer on demand”. Yet, in 2012 students in a graduate level Marine Ecology course at Harbor Branch

Oceanographic Institute at Florida Atlantic University (HBOI at FAU) observed the hermit crab Clibanarius vittatus exhibiting aggression towards the marine gastropod Melongena corona in the field. A laboratory study indicated a novel interaction: Clibanarius vittatus killed and obtained shells directly from live

Melongena corona (Kennedy et. al., Unpublished Manuscript). This finding is converse to the work of Laidre (2011) who found that both a marine (Pagurus bernhardus) and a terrestrial (Coenobita compressus) hermit crab species were physically incapable of removing any of five different species of live gastropods from their shells. In addition, fewer than 6% could remove dead intact gastropods from their shells. Gastropod fatality caused by a hermit crab has been recorded 1

only once in an aquarium setting and the two species involved did not occur naturally in the same range (Rutherford, 1977).

1.1. Evolutionary and Ecological Significance

The ability of a hermit crab to directly acquire a shell from a gastropod has both ecological and evolutionary significance. Ecological effects on the system will be regulated by the driver of this interaction. Two of the most common interspecies interactions are predation and competition. However, the interaction described above between Clibanarius vitattus and Melongena corona (hereafter both species will be referred to by their generic names) does not fit either definition. In predation, one organism is driven to kill another because of the need for a food source. Competition is driven by two organisms that both require the same limited resource in order to survive. This study is designed to determine the driver of the interaction between Clibanarius and Melongena so that it may be properly classified.

A variety of factors may influence the interaction between these two species. Hermit crab populations are limited by the availability of adequate shells which are normally low in abundance (Kellogg, 1976; Scully, 1979; Tricarico et al., 2009). Studies conducted around the world including Massachusetts

(Thompson, 1903), Costa Rica (Childress, 1972), Bermuda (Provenzano, 1960),

Hawaii (Reese, 1969; Hazlett, 1970), and Florida (Bach et. al., 1976) report a scarcity of shells of all sizes available for hermit crab use. Additional studies carried out in the Black Sea (Drapkin, 1963), Hawaii (Reese, 1969), Norway

(Samuelson, 1970), and Washington (Vance, 1972) reported a scarcity of large shells specifically. Availability of shells is affected by both their natural abundance in the habitat and inter- and intraspecific competition (Reese, 1969).

The notion of overall shell scarcity is supported by observations that occupied shells are often severely damaged or of suboptimal size (Hazlett, 1970;

Childress, 1972; Vance, 1972b) and the fact that hermit crabs sometimes use objects other than shells for protection (Balss, 1924; Provenzano, 1968).

Furthermore, additions of empty shells seem to increase hermit crab density

(Vance, 1972a) and maximum size (Drapkin, 1963).

The ability to kill and obtain a shell directly from a gastropod provides a large evolutionary advantage to a hermit crab. This ability would increase the likelihood of obtaining an adequate shell and thus the species may outcompete other hermit crab species as well as other organisms which utilize gastropod shells such as certain species of fish (Springer et. al., 1961), octopus (Mather,

1972), and tanaidaceans (McSweeny, 1982). If Clibanarius can obtain shells directly from Melongena, then it has a greater number of available shells to select from and as a consequence Clibanarius population growth would be likely.

Hermit crab survival is dependent on the efficacy of the shell they inhabit.

Crabs that can withdraw completely into their shells are more likely to escape predation and shells decrease desiccation by controlling evaporation and body temperature (Reese, 1969). In addition, the shell regulates growth and reproduction (Markham, 1968; Childress, 1972; Fotheringham, 1976; Hazlett,

1981). For these reasons, shells must meet a number of criteria in order to be an

adequate form of protection for a hermit crab. It is essential for a hermit crab to obtain a shell that fits properly, namely, one that is the appropriate size for its body (Turra and Leite, 2002). A shell that is too large will decrease a crab’s locomotive abilities, making it more vulnerable and reducing the chances of survival (Childress, 1972; Bertness, 1981; Ohmori et al., 1995; Wada et al., 1997;

Arguelles et al., 2009). However, if a shell is too small it can lead to an increased risk of predation, mechanical damage, desiccation, and removal by a more aggressive hermit crab. It has been demonstrated that for at least seven species of hermit crabs that growth is reduced in a shell that is too small (Bertness, 1981;

Fotheringham, 1975; Nyblade, 1974; Markham, 1968).

Shell size and fit also affect reproduction. Hermit crabs with large shells have increased reproductive success because of increased likelihood of copulatory success (Hazlett, 1989; Hazlett & Baron, 1989). In addition, large shells provide an increase in available brood space in females while small shells potentially reduce fecundity (Glassell, 1937; Reese, 1969; Ameyaw-Akumfi,

1975; Bach et. al., 1976; Fotheringham, 1976; Bertness, 1981a; Elwood et al.,

1995). For male Clibanarius, obtaining a large shell is necessary for protection and survival as they are typically larger in size (Markham, 1968; Werner, 1972;

Trivedi and Vachhrajani, 2014).

A shell may also be considered inadequate because of its condition. If the aperture is blocked or sealed by sand grains, shell fragments, or fouling organisms the hermit crab will not be able to enter the shell. Broken or damaged shells are likely to provide inadequate protection from predators or hinder the

hermit crab from effectively gripping the shell while moving (Kellogg, 1976).

There is also evidence that some hermit crab species prefer shells from specific species of gastropods (Kellogg, 1976; Vance, 1972b).

Hermit crabs have evolved sophisticated behavioral and sensory adaptations to select and obtain optimal shells (Rittschof et al. 1995, Hazlett

1996a, 1996b, Tricarico et al. 2009). Inspection of an empty gastropod shell normally involves a complicated set of behavioral acts such as positioning of the shell and insertion of the chelipeds and first pair of walking dactyls into the aperture (Mclean, 1974). This allows the hermit crab to gather both visual

(Kinosita & Okajima, 1968) and tactile information (Reese, 1963; Scully, 1983;

Elwood & Stewart, 1985). They have also been shown to learn from past results of obtaining shells, allowing them to adapt and become more likely to obtain an optimal shell resource as time passes (Elwood et al., 1979; Hazlett, 1992). Shell switching between healthy hermit crabs also occurs when there is potential for both individuals to benefit. In 78% of shell switching incidences observed by

Hazlett (1996) both hermit crabs involved benefitted and obtained an improved shell resource. Hermit crabs also have evolved the ability to detect chemical cues produced by gastropods and conspecifics that are injured or dying, thus they can locate shells that are currently occupied, but may soon become empty, (McLean,

1974; Hazlett, 1996b; Orihuela et. al., 1992; Rittschof et. al., 1992). These chemicals specifically signal the availability of a shell and do not evoke a feeding response (McLean,1975; Rittschof, 1980a; Gilchrist, 1984; Orihuela et. al., 1992;

Rittschof et al., 1992). We hypothesized that the interaction between Clibanarius

and Melongena may also give Clibanarius access to considerably larger shells, however availability of large shells may remain limited due to the energy required to obtain this resource. The benefit-to-cost ratio theory states that if the costs of an action are greater than the benefits, natural selection will select against that action (Ha, 2010). While large shells may provide the greatest benefit to

Clibanarius, it may require more energy than Clibanarius has available to successfully kill a large Melongena and obtain its shell. Laidre (2011) hypothesized that it would require a substantial amount of force, and therefore energy, in order to remove a snail from its shell.

1.2. Clibanarius vittatus and Melongena corona

Clibanarius vittatus is a marine hermit crab found in temperate, subtropical, and tropical habitats as far north as the Potomac River in Virginia on the eastern coast of the U.S. to as far south as the Rio de Janeiro in Brazil

(Young, 1978; Lowery and Nelson, 1988; Mantelatto et al., 2010). Distribution is limited by larval salinity requirements (Kelly and Turner 2011, Lowery and Nelson

1988). Larval survival and rate of development in Clibanarius is optimal at high salinities and moderate temperatures. A study conducted by Young and Hazlett

(1978) found complete development of juveniles only occurred at combinations of

0 25 and 30 /00 salinity with 25 and 30°C temperatures. This study was supported by population surveys conducted in 2011 by Kelly and Turner that recorded

Clibanarius populations only in areas of consistently high salinity. Once reaching adulthood, Clibanarius are considered salinity tolerant but prefer habitats with a

0 salinity between 20-30 /00 (Young and Hazlett, 1978). Adults are also tolerant of desiccation. Young (1978) found that naked Clibanarius could spend an average of 158 minutes in a desiccator before mortality occurred. While Clibanarius is considered a habitat generalist, large populations are found in locations with sandy substrate and mangroves (Coehlo and Ramos, 1972; Williams, 1984).

Melongena corona is a marine gastropod found in tropical and subtropical habitats on both coasts of the Florida peninsula, eastern Alabama, and throughout much of the West Indies as far south as South America. Melongena larvae are more salinity tolerant than those of Clibanarius, however larval

0 mortality increases when salinity falls below 15 /00 (Garland and Kimbro, 2015).

As adults Melongena can tolerate low and variable salinities but remain sensitive to low temperature (Hathaway 1957, Loftin 1987) and desiccation (Hamilton

1996). Melongena often bury into the sediment and it is hypothesized this affords protection from these stressors. Adult Melongena are highly predatory snails which consume oysters, clams, and other crown conchs, and additionally scavenge dead invertebrates and fishes (Menzel and Nichy 1958; Garland and

Kimbro, 2015). For this reason large populations of Melongena have been associated with oyster reefs as well as areas with hard or rocky substrate

(Menzel & Nichy 1958, Hathaway & Woodburn 1961) as they require a hard substrate on which to lay their eggs.

If population density varies with habitat type this may cause interactions between the two species to differ among habitats. High Clibanarius population densities may drive direct shell acquisition from Melongena as shell switching

could allow a large number of Clibanarius to benefit. In addition, populations with various Melongena densities may respond differently. If the addition of one new shell adequately provides for the need of a large number of Clibanarius,

Melongena populations with high density may not be largely affected.

1.3. Objectives and Hypotheses

The objective of this study was to systematically demonstrate that

Clibanarius have the ability to kill and obtain shells directly from Melongena which may provide evolutionary advantages. In addition, this study investigated potential drivers of this novel interaction in order to identify the interaction. It is expected that results from this study will shed light on the ecological effects of this interaction. To accomplish these objectives, this study contained three components as described below.

1.3.1. Manipulative Lab Experiment

Previous research demonstrates shell resources increase fitness

(Markham, 1968; Childress, 1972; Fotheringham, 1976; Hazlett, 1981)

and provide different benefits to the sexes (Fotheringham, 1976; Bertness,

1981a; Elwood et al., 1995; Trivedi and Vachhrajani, 2014). However,

acquiring this resource requires an expenditure of energy. Accordingly, the

manipulative lab experiment was designed to address three hypotheses:

(1) Male Clibanarius kill and obtain shells from Melongena at a higher rate

than females, (2) the size of Melongena and Clibanarius will affect the outcome of this interaction, and (3) Clibanarius shell characteristics including condition, species, and fit will impact the result of this interaction.

1.3.2. Manipulative Field Experiment

Hermit crab populations are limited by the availability of adequate shells which are normally low in abundance (Kellogg, 1976; Scully, 1979;

Tricarico et al., 2009). The manipulative field experiment was designed to address the hypothesis that Clibanarius and Melongena interactions vary based on population densities.

1.3.3. Field Surveys

Little is known regarding habitat preference and population sizes of these organisms near the area where this interaction was observed. Field surveys were conducted to address the hypothesis that habitat type will impact population densities and sizes of Clibanarius and Melongena and cause interactions between these two species to vary.

2. MATERIALS AND METHODS

2.1. Study Species and Locations

Clibanarius vittatus and Melongena corona were chosen for this experiment as Clibanarius has been observed exhibiting aggression towards

Melongena in areas of the Indian River Lagoon (IRL) (Kennedy et. al.,

Unpublished Manuscript). The IRL is an estuary that runs along the eastern coast of Florida, United States, from Ponce de Leon Inlet in the north to Jupiter inlet in the south (~ 28.7° to 27.2° N), a distance of approximately 174 km. The range of

Clibanarius and Melongena overlap in many locations (including the IRL) where both species are abundant in intertidal and subtidal areas. The intertidal zone is a harsh environment. Organisms must be able to tolerate intense environmental factors such as abrasion caused by wave action, desiccation, and exposure to a wide range of salinities and temperatures (Reese, 1969; Coelho & Ramos, 1972;

Williams, 1984; Kelly & Turner, 2011). Shells provide an extra layer of protection from these physical factors and also protect against predation, which is important as they are also often exposed to both marine and terrestrial predators (Reese,

1969). There are also advantages to living in this habitat. Due to waves and tidal flux, the intertidal zone is continuously supplied with organic material providing an easily accessible food source (Reese, 1969).

Experiments were conducted at Harbor Branch Oceanographic Institute at

Florida Atlantic University (HBOI at FAU) and Clibanarius were gathered locally in Fort Pierce, Fl. Melongena populations were not sufficiently large in local areas of the IRL near HBOI. For this reason they were collected from a larger population approximately 143 km further north in the IRL (Cocoa, Fl) (Fig. 1).

Melongena were transported about an hour and a half to HBOI at FAU. At the conclusion of the experiments living organisms were returned to the IRL. The manipulative field experiment was carried out during Jun- July 2016, the manipulative lab experiment was carried out during Sept- Nov 2016, and field surveys were conducted from May- Oct 2016.

Figure 1: Map of locations utilized within study including Cocoa (28°24'13"N, 80°39'42"W), H.B.O.I. at FAU (27°32'10" N, 80°20'59 W), and Fort Pierce (27°28'25"N 80°19'19"W).

2.2. General Experimental Protocol

For the lab and field experiments all organisms were measured prior to initiation of the study. Melongena utilized had shell lengths 10-20% larger than

Clibanarius individuals they were paired with. This methodology was based on a previous study which found, on average, Clibanarius killed Melongena with a shell length 10- 20% larger than that which Clibanarius originally occupied

(Kennedy et. al., Unpublished Manuscript). All Clibanarius individuals within an experimental unit had a similar shell length. Shell length was measured as the

distance from the tip of the apex to the tip of the siphonal aperture (Dalby, 1989).

Utilizing larger Melongena ensured that the Clibanarius had the potential to acquire an improved shell habitat. Below the experimental design is detailed for each hypothesis addressed.

2.3. Manipulative Lab Experiment: Drivers of Shell Acquisition

This experiment was conducted to test the following three hypotheses:

1. A higher number of male Clibanarius will kill and obtain a shell from

Melongena than female Clibanarius.

2. Size of Melongena and Clibanarius will affect the outcome of this

interaction.

3. Clibanarius shell characteristics including species, condition, and fit will

affect the outcome of this interaction.

In this experiment, one Melongena individual was placed in each of 40 small low-density polyethylene containers (32 x 17 cm, 14 cm height). Containers were filled two thirds of the way with sea water (approximately 5 liters, 35 psu) and fitted with a perforated snap-top lid and an air stone (Fig. 2). Water temperature was not regulated and varied with the room (estimated variation of

23- 29⁰C). To account for differences caused by the spatial arrangement of the containers a four block design was utilized. Five containers out of the ten within each block were randomly chosen and three Clibanarius individuals were added to these containers (Fig. 3).

Figure 2: Polyethylene (LDPE) Figure 3: Random arrangement of treatment containers arranged for the groups within blocks. Each color represents a manipulative lab experiment. separate block. “M” represents the containers with Melongena only and “B” represents the containers with both Melongena and Clibanarius.

At experiment initiation, shell characteristics including species, condition, and fit were recorded for all Clibanarius. Shell condition was recorded as either broken, chipped, or undamaged. Shells that were considered broken had serious, shape altering damage (missing a portion greater than 5 mm2). Shells considered chipped had minor damage that did not alter the overall shape

(missing a portion less than 5 mm2). Shells considered undamaged had negligible damage or were completely intact. Shell fit was assigned using methods adapted from Turra 2003. Hermit crabs were gently prodded and their ability to retreat within their shells was used as a measure of shell fit (Table 1).

Ability to Retreat Visibility Assigned Shell Fit Complete No portion of the body visible Good Partial Dactyls visible Fair Partial Dactyls and chelipeds visible Poor Table 1: Methods used to assign Clibanarius shell fit. Adapted from Turra 2003.

This experiment was conducted for 35 days and each day* the containers were examined for Melongena mortality (*the experiment was paused for six days due to hurricane Matthew and Clibanarius and Melongena organisms were separated). When Melongena mortality occurred, carcasses separated from shells were collected. In addition, the Clibanarius individual who successfully obtained the Melongena shell was separated from those who were unsuccessful.

This prevented shell switching between successful and unsuccessful Clibanarius individuals. Examinations were conducted at approximately the same time each day to maintain consistency throughout the experiment.

Throughout the experiment, Clibanarius and Melongena were placed in separate containers twice each week and allowed to feed until satiation on frozen

Great Value brand Tilapia (farm raised in China). After feeding, water was changed in all containers to prevent water fouling. Prior to this experiment, a preliminary test was conducted to determine preferred food type. Clibanarius and

Melongena individuals in separate containers were offered a single type of food.

Foods tested included various types of marine pellets (varying densities and sizes), vegetative material, and frozen tilapia. After a period of 24 hours, both

Melongena and Clibanarius in containers with frozen tilapia had eaten while other food sources remained untouched. For this reason it was chosen for the experiment.

At the conclusion of the experiment all Clibanarius were removed from their shells using non-lethal methods adapted from Pechenik et. al. (2015).

Clibanarius were subjected to water of approximately 40ᵒ C causing partial 15

emergence from the shell. Clibanarius were then guided out of the shell by gently applying downward pressure to the carapace using the thumb and forefinger.

Immediately after shell removal Clibanarius were returned to room temperature sea water for cephalothorax measurement and sex determination. To the knowledge of the author, the differences between male and female have not specifically been recorded for the species Clibanarius vittatus. Some species of male hermit crabs possess pleopods while some do not (Coenobita clypeatus).

Dr. Richard Turner, a Clibanarius expert, assisted in ensuring the correct sexual identification. Females were identified by the presence of gonopores on the third pair of walking legs and large, well-developed pleopods (Fig. 4a & b).

Conversely, males were identified by the absence of gonopores on the third pair of walking legs and small, poorly-developed pleopods (Fig. 4c & d). Once these observations were completed, Clibanarius were allowed to return to their shells.

A B

C D

Figure 4: Photos A and B are females and D and C are males. A- Abdomen with gonopores located at the base of the third pair of walking legs (circled). B- The tail portion of the abdomen featuring large, well-developed pleopods. In females, pleopods are primarily utilized for holding eggs (Ingle 1993, Fantucci et. al. 2009). C- Abdomen with gonopores absent from the base of the third pair of walking legs. D- The tail portion of the abdomen with small, poorly developed pleopods. In males, pleopods are used for circulating and aerating water in the shell (Fantucci et. al. 2009).

After data collection, two sets of survival analyses were conducted (SAS,

University Edition, SAS Institute, Cary, NC, U.S.A.). The first set analyzed whether blocks, treatment, or Melongena size had an effect on the amount of time until Melongena was killed and removed from its shell (Table 2). The second set analyzed whether Clibanarius sex, size, or shell characteristics (species, condition, and fit) had an effect on the amount of time required for Clibanarius to kill and remove Melongena from its shell (Table 3). A survival analysis was chosen because other analyses do not take into account the timing of the

response variable. In addition, repeated observations on the same subject, as were conducted in this experiment, are not independent and a survival analyses are designed to handle this type of data. There were no significant differences between blocks, and for this reason all units within a treatment were pooled for further analysis.

A B

Independent Variable Dependent Variable

F Blocks B i Treatment Time until Melongena death Melongena size g Tableu 2: First set of survival analyses conducted for the manipulative lab experiment. Melongena sizer refers to Melongena shell length.

e 5

: Independent Variable Dependent Variable P Cephalothorax Length Clibanariusl characteristics Sex a Time until Clibanarius Species c obtained a new shell e Shell characteristics Condition m Fit Tablee 3: Second set of survival analyses conducted for the manipulative lab experiment. n t a 2.4.n Manipulative Field Experiment: Interactions between Melongena and d Clibanariusa vary based on Population Density r r a This experiment was conducted to test the hypothesis that Clibanarius and n Melongenag interactions vary based on population densities. The experiment was e m carriede out in a shallow subtidal area of the Indian River Lagoon directly n accessiblet from HBOI at FAU (27°32'10" N, 80°20'59 W). A total of twenty o enclosuresf were designed to contain established densities of Melongena and e Clibanariusn and exclude any individuals naturally present in the environment. c l o 18 s u r e s

Enclosures were placed parallel to the shoreline approximately two meters below the low tide line on June 29th 2016 (Fig. 5 & 7). This placement exposed the enclosures to an environment with low wave energy and maximum water depth that ranged from approximately 0.5- 0.75 m. Although the enclosures were originally placed two meters past the low tide line, on most days they were in the intertidal zone, and minimum water depth ranged from approximately 0- 0.25m.

The enclosures were approximately one meter apart and buried about 5 cm into the sediment to anchor them in place.

Figure 5: Placement and arrangement of enclosures in the field.

Enclosures were constructed of four inflexible ½ m X ½ m panels of 6 cm2 plastic mesh that were zip-tied together (0.25 m2) (Fig. 6). The large mesh size allowed for adequate water flow through the cages. A ½ x ½ m panel of 0.5 cm2 plastic mesh was secured to completely cover the top of the enclosure using a combination of zip-ties and plastic coated garden wire. Using garden wire allowed the top to be opened and closed repeatedly. PVC poles were attached around the interior perimeter of the cages approximately 25 cm above the sediment surface. This prevented Melongena from climbing the cage sides 19

(Clibanarius climbing was not inhibited by the PVC). The bottom of the cages were open, thus Melongena were free to burrow into the sediment.

Figure 6: Close up of the enclosure with the ceiling removed.

Four treatments were developed utilizing combinations of low and high densities of both Melongena and Clibanarius. Low density included one organism per enclosure (4 m-2) and high density included four organisms per enclosure (16 m-2) (Table 4). These densities are high compared to average densities recorded during surveys. However, Melongena and Clibanarius often form aggregations in the field that are consistent with these densities (Cutter and Devlin, Personal

Observations). A fifth treatment contained neither Clibanarius nor Melongena to test for caging effects. Each treatment was replicated four times and randomly assigned to the twenty enclosures.

Treatments

1 2 3 4 Empty Melongena Density Low High Low High 0 Clibanarius Density Low Low High High 0 Table 4: Densities of Melongena and Clibanarius utilized for experimental treatments. Low densities included one organism per enclosure (4 m-2) and high densities included four organisms -2 per enclosure (16m ). The last treatment utilized empty cages to test for caging effects.

Figure 6: Arrangement of enclosures based on a random design. Numbers correspond to treatments in table 4. Figure not to scale. 0: Enclosures devoid of organisms; 1: Low Melongena & Low Clibanarius (1M: 1C); 2: High Melongena & Low Clibanarius (4M: 1C); 3: Low Melongena & High Clibanarius (1M: 4C); 4: High Melongena & High Clibanarius (4M: 4C).

This experiment was designed to determine if the outcome of the interaction between Melongena and Clibanarius varied based on population density. However, despite initial testing, enclosures were not impervious to

Clibanarius immigration and emigration and thus Clibanarius densities varied.

While this was unplanned, it allowed the relationship between the number of

Clibanarius that gained access to the enclosures and the treatment type to be analyzed. In addition, analysis was conducted to determine if the rate of change in Clibanarius affected Melongena mortality rate. The experiment was conducted for 20 days and the enclosures were observed five days a week approximately 1-

2 hours before low tide. During each observation four variables were measured and recorded: (1) number of living Melongena and Clibanarius in each enclosure,

(2) apparency of each individual (buried or exposed), (3) number of Melongena individuals being attacked by Clibanarius, and (4) number of Clibanarius 21

gathered around the outside of the enclosure. Clibanarius around the enclosure was recorded as there were often individuals attempting to gain access to the enclosures. This was especially noticeable when Clibanarius within the enclosures were in the process of removing a Melongena individual from its shell.

Clibanarius within a ½ meter of the cage was considered near the enclosure, however, most were within about 10 cm of the enclosure (Fig. 8).

Figure 8: Eight Clibanarius gathered around an enclosure.

Statistical analyses were performed with SAS (University Edition, SAS

Institute, Cary, NC, U.S.A.) to determine whether the change in Clibanarius presence within the cages, hereafter referred to as Clibanarius attraction, and

Melongena mortality significantly varied among the treatments. Clibanarius attraction throughout the study period was analyzed using a multivariate analysis of variance (MANOVA). Collecting data repeatedly over a period of time creates multiple dependent variables and a MANOVA analysis accounts for this.

Established density of Melongena and Clibanarius was utilized as the independent variable. The ratio of the number of Clibanarius actually present

within the enclosures compared to the number of Clibanarius that had originally been established within the enclosures was utilized as a response variable. The amount of time passed since initiation of the experiment, in days, was utilized as a secondary response variable. For days in which the MANOVA test indicated a significant difference between treatments, a protected analysis of variance

(ANOVA) was conducted to determine how the density treatments significantly differed.

Melongena mortality throughout the study was analyzed using a

MANOVA. Established density of Melongena and Clibanarius was utilized as the independent variable. The ratio of the number of Melongena actually present within the enclosures compared to the number of Melongena that had originally been established within the enclosures was utilized as a response variable. The amount of time passed since initiation of the experiment, in days, was utilized as a secondary response variable. Individual ANOVAs were not conducted because significant differences were not found when data were analyzed using MANOVA.

2.5. Field Surveys: Effect of habitat on population densities and sizes of

Clibanarius and Melongena

Field surveys were conducted to test the hypothesis that the presence and size of Clibanarius and Melongena vary with habitat. Five surveys were conducted 1-2 hours before low tide in subtidal areas of the Indian River Lagoon

(IRL) between May and October of 2016. Surveyed habitats included both hard, rocky shoreline and mangrove shoreline (Fig. 9). Clibanarius and Melongena are 23

often observed in these habitats and it is hypothesized that there may be a variation in Clibanarius and Melongena population demographics between them.

Surveys were conducted at three separate locations within the IRL (Fig. 1). Two local locations (HBOI and Fort Pierce) were chosen as prior observations indicated Clibanarius populations may be larger than Melongena populations in these areas (Cutter and Devlin, Personal observations). A northern location

(Cocoa) was chosen as prior observations indicated Melongena populations may be larger than Clibanarius populations in this area (Cutter and Devlin, Personal observations). These surveys also allowed for comparisons between location in the IRL. In two of these locations (HBOI and Fort Pierce) both mangrove shoreline and hard, rocky shoreline existed, and two separate surveys were conducted for each habitat type. Mangrove shoreline was the only habitat type at the Cocoa survey location and only one survey was conducted.

Figure 9: Shoreline habitats chosen for surveys. Left- Mangrove shoreline. Right- Hard substrate/

rocky shoreline.

At each of the five survey sites two 50 meter long transects were established. The primary transect was located approximately 1 meter past the low tide line while the secondary transect was located approximately 4 meters past the low tide line. The occupant of every gastropod shell within 1 meter of each transect was identified and the length of the shell was measured. For hermit crabs encountered, shell condition, fit, and species were also recorded using the same indices used for the manipulative lab experiment.

To adequately address the hypothesis, additional surveys were planned.

Unfortunately, because of weather and logistical issues, only two sites with a rocky shoreline and three sites with a mangrove shoreline were surveyed as previously described. Due to low replication, it was not possible to statistically analyze differences between the two habitat types. Instead, statistical analyses were performed (SAS, University Edition; SAS Institute, Cary, NC, U.S.A.) to determine if the presence and sizes of Clibanarius and Melongena varied among the five conducted surveys. Organism type (including both shell occupant and shell species) was analyzed using a chi-square test as the data was categorical in nature. This test assumes data values are large. As most recorded data values were small, Chi-Square results were asymptotic and the Monte Carlo Estimate for the Exact Test was utilized. Exact tests compare two proportions and are based on calculations of exact probabilities. The Monte Carlo method is a repeated sampling method that provides an unbiased estimate of the exact P value when a chi-square test produces asymptotic results. Continuous data (shell length) was analyzed using an ANOVA. A statistical analysis was also performed

to determine if there was a relationship between Clibanarius shell species and shell fit for surveyed individuals. Chi-Square results were again asymptotic and the Monte Carlo Estimate for the Exact Test was utilized.

3. RESULTS

3.1. Manipulative Lab Experiment: Drivers of Shell Acquisition

The results of this experiment indicate that sex does not significantly affect the outcome of this interaction (P= 0.2089, Table 5). An equal percentage of male and female Clibanarius killed and successfully obtained a new shell from

Melongena (Fig. 10). In addition, organism size and the condition and species of the original shell inhabited by Clibanarius in the experiment were not significantly related to the outcome of this interaction (Table 5). Rather, Clibanarius shell fit drives this interaction. A significantly higher number of Clibanarius which inhabited a shell with a poor fit (shell was too small and did not allow crab to fully retreat) killed and obtained a new shell from Melongena than those that had a fair or good shell fit (P < .0001, ANOVA, Table 5) (Fig. 11). In all instances, the new shell acquired offered an improved shell fit.

It is important to note that there was a significant difference in Melongena mortality when Clibanarius was present (P= 0.0001, Survival Analysis, Table 5).

Only 1 Melongena perished when Clibanarius were not present while 12 were killed (but not consumed) when Clibanarius was present. This confirms that

Clibanarius negatively impact Melongena survival (Fig. 12).

Degrees of Pr > Chi- Variable Chi-square Freedom Square Clibanarius Sex 3.1319 2 0.2089 Melongena Shell Length 3.7565 2 0.1529 Clibanarius Shell Length 1.4766 2 0.4779 Clibanarius Cephalothorax Length 10.7277 2 0.0047* Clibanarius Shell Width 2.4397 2 0.2953 Clibanarius Shell Species 2.6007 5 0.7613 Clibanarius Shell Condition 0.4233 2 0.8092 Clibanarius Shell Fit 29.1571 2 <.001 Treatment 14.5160 1 0.0001 Table 5: Results from survival analyses conducted to determine if Clibanarius sex, organism size, or Clibanarius shell characteristics (species, condition, and fit) affect the outcome of this interaction. * After adjusting for covariance using the Wilcoxon test shield length became insignificant (P = 0.4090).

Sex of Clibanarius that Killed Shell Fit of Clibanarius that Killed Melongena Melongena 100 100 90 90 80 80 70 70 60

Clibanarius 60 Clibanarius 50 50 40 40 30 30 20 20

10 Percentage Percentage of

Percentage Percentage of 10 0 Male Female 0 Good Fair Poor Clibanarius Sex Clibanarius Shell Fit Figure 10: Percentages of male and female Clibanarius that killed Melongena to obtain a Figure 11: Percentages Melongena killed by shell according to shell fit (P= .2089). In four Clibanarius to obtain a shell (P< 0.001). In individuals (33%) sex could not be three individuals (25%) shell fit could not be determined. determined.

Figure 7: Percentages of male and female Clibanarius that killed Melongena to obtain a shell according to shell fit (P= .2089). In four individuals (33%) sex could not be determined.

Melongena Mortality by Treatment

100 90

Melongena 80 70 60 50 40 30 20 10 0 Melongena Alone Clibanarius and

Percentage Percentage of Deceased Melongena Treatment

Figure 12: Percentages of Melongena killed by Clibanarius to obtain a shell (P= 0.0001)

Throughout the experiment the behavior of Clibanarius while killing and removing Melongena from their shells was observed. Clibanarius positioned themselves in front of Melongena so that the aperture of its shell was lined up with the aperture of the Melongena shell (Fig. 13). Clibanarius then appeared to insert its chelipeds and dactyls under the operculum of the Melongena and push it out of the way to the extent that it had space to crawl into the shell alongside the snail tissue. At this point both the Melongena snail and the Clibanarius individual were in the shell together (Fig. 15). Finally, Clibanarius appeared to

“cut” Melongena out of the shell and once the tissue was completely detached, push it out from behind. After the Melongena carcass was removed, Clibanarius was never observed to consume the Melongena tissue and the carcass remained completely intact (Fig. 14). This indicates that Clibanarius are killing Melongena to obtain an improved shell resource, and not to obtain a food source.

Figure 83: Clibanarius positioned to remove Figure 14: An intact Melongena individual that Melongena from its shell with both apertures was killed and removed from its shell by of the shells aligned. Clibanarius.

Figure 9: Clibanarius positioned to remove Figure 10: An intact Melongena individual that Melongena from its shell with both apertures was killed and removed from its shell by of the shells aligned. Clibanarius.

Figure 15: Clibanarius and Melongena simultaneously in the Melongena shell.

3.2. Manipulative Field Experiment: Interactions between Melongena and

Clibanarius vary based on population density

This experiment indicates that Clibanarius attraction significantly varies with Melongena and Clibanarius density (P <.0001, MANOVA, Table 6).

Clibanarius attraction to enclosures with a high Melongena / low Clibanarius density (4M: 1C) was significantly greater than Clibanarius attraction to enclosures with low Melongena / high Clibanarius density (1M: 4C) for the majority of the experiment (days 6- 20). On days 12 and 14 Clibanarius attraction was also significantly greater to enclosures with low Melongena / low Clibanarius density (1M: 1C) than to enclosures with low Melongena / high Clibanarius (1M:

4C) density (Fig. 16). Despite variations in Clibanarius attraction Melongena mortality rates did not significantly vary between treatments (P =0.9035,

MANOVA, Table 6) (Fig. 17). In summation, rate of increase in Clibanarius presence varied significantly among the original treatments. However, in this case, Clibanarius density did not significantly affect the rate of Melongena mortality.

Out of 40 total Melongena utilized in this experiment, 36 experienced mortality after 20 days. Enclosures utilized in this experiment did not have bottoms, therefore Melongena were free to bury in order to avoid mortal interactions with Clibanarius and 80% of the Melongena were observed to bury under the sediment during the course of this experiment. However, this tactic does not appear to increase the chances of Melongena survival as 90% of individuals perished by the end of the experiment.

F Value Num DF Pr > F Clibanarius Infty 60 <.0001 Attraction Melongena 0.46 36 0.9035 Mortality Table 6: Results of two MANOVAs (Wilks Lambda) comparing Clibanarius attraction and Melongena mortality to various population densities.

Figure 116: Ratio of the observed number of Clibanarius within each enclosure to the initial number established within each enclosure. As the MANOVA indicated an overall significance in Clibanarius attraction with density, individual protected ANOVAs were performed for each day. Treatments with the same letters within a single day are statistically the same based on Tukey’s a-posteriori comparisons. All treatments are statistically the same for days devoid of letters. Error bars represent standard error. Data shown are untransformed for clarity. This indicates the rate of increase in Clibanarius presence significantly varied among the original treatments established.

Figure 127: Ratio of the observed number of Melongena within each enclosure to the initial number established within each enclosure. Error bars represent standard error. No significant difference was found among any treatments at any time step. This indicates the rate of Melongena mortality does not vary based on Clibanarius attraction (P <.9035, MANOVA).

3.3. Field Surveys: Effect of habitat on population densities and sizes of

Clibanarius and Melongena

Surveys indicate that there is a significant relationship between organism type and site (P< 0.0001, M.C. estimate for the exact test, Table 7). As both variables are categorical, it was not feasible to determine statistically which variables differed from each other. However, several trends can be seen within the data. Primarily, there appears to be more variation among mangrove habitats than between mangrove and rocky habitats. In mangrove habitats, Clibanarius and empty shells were found at two sites (Fort Pierce and HBOI) while live

Melongena and empty Melongena shells were found only at the most northern

site (Cocoa). In rocky habitats, Clibanarius were the most common shell inhabitant at all sites surveyed. In addition, there is a fairly large variation in the number of shells found at each of the three mangrove habitats (Fig. 18). At both mangrove and rocky habitats in Fort Pierce and HBOI, most shells encountered were occupied by Clibanarius. In addition, Busycon spiratum and Melongena corona were the most common shell species recorded for all sites regardless of habitat type (Fig. 19). Interestingly, live Clibanarius and live Melongena were never observed together at any site.

Pearson Chi- Square Test

Variables Chi- Degrees of Asymptotic M.C. Estimate for Exact Test Square Freedom Pr> ChiSq Pr > ChiSq Organism Type and 170.0956 60 <.0001 <.0001 Survey Site Shell Species and 40.1739 24 0.0205 0.0780 Clibanarius Shell Fit Table 7: Results from Pearson Chi-square test for categorical variables recorded during field surveys including asymptotic chi-square and Monte Carlo estimate for the exact test. Chi-square results were asymptotic and the Monte Carlo estimate for the exact test. Chi-square results were asymptotic and the Monte Carlo estimate for the exact test was utilized. Organism type includes both shell occupant (Clibanarius, Melongena, or no occupant) and shell species.

Shell Occupants by Survey Site

40 35 30 25 20 15 10 5

NumberofIndividuals 0 Ft. P. H.B.O.I. Ft. P. H.B.O.I. Cocoa Rocky Mangrove

Survey Location and Habitat Type

Empty Clibanarius Melongena

Figure 138: Comparison of shell occupants at each surveyed site (P<.0001, M.C. estimate for exact test).

Figure 149: Comparison of shell species at each surveyed site (P<.0001, M.C. estimate for exact test). Species are abbreviated according to table 5 below.

Abbreviation Species Common Name BS Busycon spiratum Pear Whelk MC Melongena corona Florida Crown Conch PD Polinices duplicatus Lobed Moon Snail BP Busycon perversum Lightning Whelk SF Stramonita floridana Rock snail NU Nerita undata Wave Marked Nerite FT Fasciolaria tulipa True Tulip OS Oliva sayana Lettered Olive UK Unknown Unknown Table 8: Abbreviations utilized for snail and shell species.

Surveys did not indicate a significant relationship between shell fit and shell species (P= 0.0780, M.C. estimate for the exact test, Table 7). Clibanarius were found in the shells of nine different gastropod species, but the majority of

Clibanarius that had a good shell fit were found in Busycon spiratum or

Melongena corona shells (Fig. 20). This is most likely due to the fact that these shell species were the most common in the environment. Indeed, the majority of

Clibanarius that had a poor shell fit were also found in Busycon spiratum or

Melongena corona shells. Out of the Clibanarius surveyed, 50 (75%) individuals had a good shell fit while only 17 (25%) had a poor shell fit.

Clibanarius Shell Fit and Type

30 25

15 10

5 Number Individuals of 0 BS MC LW FT SF PD UK OS NU Shell Species

Good Fair Poor Empty

Figure 2015: Relationship between shell fit and type (P= 0.0780, M.C. estimate for exact test). Empty shells recorded in Cocoa were not included as Clibanarius was absent in this location. Species are abbreviated according to table 8.

Figure 16: Relationship between shell fit and type (P= 0.0780, M.C. Surveyestimate results for exactalso test).indicate Empty a significantshells recorded relationship in Cocoa were between not included shell length as Clibanarius was absent in this location. Species are abbreviated and both site (P= 0.002, ANOVA, accordingTable 9) to and table shell 8. species (P< 0.0001,

ANOVA, Table 9). Significant variance was found both within and between habitat types (Fig. 21). Within rocky habitats, shells of Clibanarius at Fort Pierce were significantly smaller than those at HBOI. Within mangrove habitats, shells of

Clibanarius at Fort Pierce were significantly smaller than those of Melongena at

Cocoa. Between rocky and mangrove habitats, shells of Clibanarius found in mangrove habitat at Fort Pierce were significantly smaller than those found in rocky habitat at HBOI. In regard to shell species, while significant variance does occur, Melongena corona was never significantly larger or smaller than any other shell species within a given site (Fig. 22). In addition, empty shells were not significantly larger or smaller than occupied shells of any species within sites

where they were recorded. It is interesting to note that the Fasciolaria tulipa shell documented was significantly larger than almost all other shell species measured.

Variable Degrees of R-Square F Value Pr > F Freedom Survey Site 3 0.250656 4.49 0.0002 Shell Species 20 0.644681 5.99 <.0001

Table 9: Results from shell length ANOVAs demonstrating a significant relationship between survey site and shell species.

Figure 2117: Relationship between shell length, site, and organism type (P= 0.0002, ANOVA). Sites with the same letters are statistically the same based on Tukey’s a-posteriori comparisons. Error bars represent standard error.

Figure 22: Relationship between shell length, site, and shell species (P< 0.0001, ANOVA). Sites with the same letters are statistically the same based on Tukey’s a-posteriori comparisons. Error bars represent standard error. Asterisks indicate only one shell of the species was recorded at that survey site. Species are abbreviated according to table 8.

4. DISCUSSION

The method of hermit crab shell acquisition has been a subject of scientific enquiry for more than a century. In 1913 Jackson pondered the question

‘Whether the crab had simply appropriated the vacant home of a deceased

[gastropod], or whether it had forcibly ejected the owner of the shell—added

“murder to piracy”—was the question to be decided’. This study was conducted to determine if the hermit crab Clibanarius vittatus has the ability to kill and directly obtain a shell from the gastropod Melongena corona. As this type of interaction has never before been documented, a variety of potential drivers were tested to determine the proper classification of the interaction and identify ecological effects.

Results confirm that Clibanarius vittatus can in fact both kill and obtain a shell from live Melongena corona. This gives Clibanarius at least two major evolutionary advantages over other hermit crab species. First, this alleviates a major population limitation by increasing the supply of shells available to

Clibanarius and likely allows for larger population sizes. Second, it provides for a greater selection of potential shells when Clibanarius switches shells. This likely increases fitness as shells control growth and reproduction of hermit crabs

(Markham, 1968; Childress, 1972; Fotheringham, 1976; Hazlett, 1981).

Our evidence shows that Clibanarius primarily kill Melongena to obtain a shell that more adequately fits its body, thus improving its ability to grow and reproduce. These results support the hypothesis that adequate shells are a valuable yet limited resource (Thompson, 1903; Balss, 1924; Provenzano, 1960;

Drapkin, 1963; Reese, 1969; Vance, 1972a; Vance 1972b; Hazlett, 1966, 1970;

Samuelson, 1970; Childress, 1972; Hazlett, 1972; Bach et. al., 1976; Hazlett,

2012). Unexpectedly, Melongena mortality did not vary with the density of

Clibanarius present and field surveys indicate that Melongena and Clibanarius populations do not vary between rocky and mangrove shorelines. These two findings suggest that this interaction may be widespread and occur when both species are present regardless of population size and habitat. This interaction likely negatively impacts Melongena population densities and limits the size of

Melongena when Clibanarius are present.

4.1. Drivers of Shell Acquisition

The manipulative laboratory experiment was designed to address three hypotheses. The first hypothesis theorized that a higher number of male

Clibanarius would kill and obtain shells from Melongena than females. Results demonstrate that sex does not significantly affect the outcome of this interaction

(P= 0.2089, Fig. 10). Females are just as likely to kill Melongena to acquire shells as males. This finding is contrary to studies of empty shell utilization which show that while shell preferences of males and females are similar (Hazlett 1981), male Clibanarius find and utilize empty shells more efficiently than female crabs 41

(Ameyaw-Akumfi, 1975; Bertness 1981a). Male hermit crabs also typically sequester new shells and distribute them to females over time (Bertness 1981a;

Abrams, 1988; Asakura, 1995). The ability of both sexes to obtain an improved shell resource should increase the chance of survival and growth potential as well as the likelihood of copulatory and reproductive success (Hazlett, 1989;

Hazlett & Baron, 1989).

The second hypothesis investigated the effects of organism size on the interaction between Clibanarius and Melongena. Melongena were 10- 20% larger than the Clibanarius individuals with which they were paired. There was no relationship between shell size of either organism and Melongena mortality.

Likewise, Clibanarius cephalothorax length did not significantly affect the outcome of this interaction. Clibanarius with cephalothorax lengths ranging from

17.7- 29.3 mm successfully killed Melongena whose shells ranged in length from

69.7- 81.0 mm. Thus it appears that at least for these sizes of Clibanarius, the energetic cost of killing a gastropod does not outweigh the benefits (Willmer et. al., 2005; Ha, 2010).

Laidre (2011) speculated that a hermit crab would need to produce sizable force to remove a snail from its shell. However, in this case force may not be as crucial a factor in the interaction between Clibanarius and Melongena. As described in the results section, Clibanarius does not pull Melongena from its shell. Rather Clibanarius first maneuvers themselves under the operculum. This first step likely requires force, but once under the operculum, Clibanarius appears to cut the Melongena away from its shell instead of utilizing a forceful removal

tactic (Fig. 15). Cutting the flesh away from the shell is a lengthy process during which the Clibanarius is protected from other predators by the shell of the

Melongena that it is attacking. The energy and force output required of each individual may have been decreased by pairing three Clibanarius individuals with one Melongena. In the field multiple Clibanarius are often observed attacking an individual Melongena (Personal Observations, D. Devlin, 2005-2016). This would potentially benefit all Clibanarius involved as one of the hermit crabs would abandon its present shell for the Melongena shell.

The third hypothesis investigated whether this interaction was driven by various shell characteristics including species, condition, and fit. Results indicate that Clibanarius shell species and condition do not affect the outcome of this interaction. Clibanarius used in the experiment were housed in the shells of six different species. The choice to appropriate a new Melongena shell did not vary with Clibanarius shell species or shell condition. Thus these two shell characteristics do not appear to drive this interaction. This finding is contrary to multiple studies that found that that some species of hermit crabs have shown preferences for shells of certain species (Reese, 1962; Hazlett, 1981; Elwood,

1995) and that broken shells lead to increased risk of predation and desiccation

(Hazlett 1981). This study supports the evidence that the importance of these factors varies with species. For example, brooding probability for Clibanarius tricolor and Pagurus bernhardus varies significantly with shell species (Bach et al, 1976; Elwood et. al., 1995) but not for Clibanarius zebra (Hazlett, 1989).

Clibanarius vittatus shell fit does significantly affect this interaction.

Clibanarius in shells that were not large enough to offer adequate protection were much more likely to attack and kill Melongena than those in shells that fit properly (P< 0.001, Fig. 11).This finding supports the commonly accepted paradigms that shell availability affects shell utilization patterns and that the relationship between hermit crabs and shell size drives shell selection (Omhari et. al., 1995; Wada et. al., 1997; Turra and Leite, 2002). Studies show that hermit crab growth is reduced in shells that are too small (Bertness, 1981;

Fotheringham, 1976; Markham, 1968; Nyblade, 1974) and that crabs whose shells do not fit properly are often more aggressive. Scully (1979; 1983) and

Rittschof et al. (1995) also support these paradigms.

Clibanarius vittatus and Melongena corona co-occur along the east coast of Florida, and the Gulf of Mexico as far south as South America (Glassell, 1937;

Menzel & Nichy, 1958; Hathaway & Woodburn, 1961; Coehlo & Ramos, 1972;

Young & Hazlett, 1978; Williams, 1984; Lowery & Nelson, 1988; Mantelatto et al.,

2010). We studied this phenomenon only over a small area within the Indian

River Lagoon. This may be a learned behavior restricted only to the area studied.

However, the driver for this interaction (limited availability of shells of the appropriate size) is universal, and there is a potential for this interaction to be widespread. We predict that this interaction may occur where Melongena can offer an improved shell resource and where there is a lack of available empty shells. Further work is needed to verify how prevalent this activity is. Based on our results, we conclude that the outcome of the interaction between Clibanarius

and Melongena is driven by the multiple benefits accrued from a better fitting shell. The benefits of gaining a better fitting shell outweigh the costs of killing and removing Melongena from its shell.

4.2. Interactions between Melongena and Clibanarius vary based on population density.

Clibanarius attraction varies significantly with density of Melongena and

Clibanarius (P <.0001, Fig. 16). Unintentionally, Clibanarius densities were allowed to vary within the enclosures. Clibanarius aggregated both inside and outside of the enclosures that housed Melongena, thus increasing the original

Clibanarius densities in treatments that contained Melongena. Melongena densities were not affected as Melongena could not escape the enclosures and additional Melongena were not attracted to the enclosures. This allowed

Clibanarius attraction, or presence, to be studied in addition to Melongena mortality rates. Hermit crabs are attracted to chemicals released from sick and injured snails (Rittschof et al., 1990; Kratt and Rittschof, 1991; Orihuela et al.,

1992; Hazlett, 1996b; Rittschof and Cohen, 2004) as well as odors from live conspecifics (Gherardi and Atema, 2005; Tricarico and Gherardi, 2006) which may have caused the observed attraction.

Within the first seven days of the experiment, a significantly greater number of Clibanarius were attracted to enclosures with high initial densities of

Melongena and low initial densities of Clibanarius (Fig. 16). Numbers of

Clibanarius attracted to those enclosures remained significantly higher

throughout the 20 day experiment. Clibanarius may have initially been attracted to enclosures with lower numbers of Clibanarius because the chance of attaining a Melongena shell may be greater when fewer conspecifics are present.

Bertness (1981a) found that interference competitions among hermit crabs often result in only the largest hermit crabs obtaining beneficial shells. Therefore, despite shell switching activities allowing many individuals to obtain a new shell

(Hazlett, 1996a), it is possible that only the top competitor will obtain a shell that is advantageous. Thus Clibanarius may have selected enclosures where fewer competitors were present. Furthermore, these findings indicate that when

Melongena aggregate, they are more likely to attract Clibanarius than a solitary

Melongena. This attraction may be facilitated by chemicals released from

Melongena damaged by Clibanarius that recruit early.

Regardless of these variations, Melongena mortality rate was not significantly affected by Clibanarius attraction and density. By the 16th day of the experiment, 75% of Melongena in all treatments (except empty control enclosures) had been killed. Overall, while Clibanarius attraction may be driven by population sizes, the final outcome of the interaction is not impacted by population densities. This suggests that a shell with an optimal fit can be provided for Clibanarius by existing Melongena populations and Melongena will be similarly affected regardless of the densities of sympatric Clibanarius populations. A caveat that needs further study is the role of burial in natural systems. It is possible that when Melongena outside of enclosures bury

Clibanarius do not wait for them to re-surface.

4.3. Effect of habitat on population densities and sizes of Clibanarius and

Melongena

Results indicate that at the sites surveyed the assemblages of organisms present are different (P<0.0001, Fig 18). Trends within these data suggest that differences are not a result of habitat type. However, due to low replication, it was not possible to specifically analyze differences between mangrove and rocky shorelines. For this reason, individual surveys were compared.

Interestingly, Clibanarius and Melongena were not found together at any the sites surveyed. Since Clibanarius kill and directly obtain shells from

Melongena, Melongena was not be expected to be apparent or present in large numbers in areas where Clibanarius was present. The most northern site in

Cocoa was the only site where Melongena were present in high densities

(Clibanarius were absent from that site). The shells of Melongena at the Cocoa site were not significantly larger than shells occupied by Clibanarius at any other site, with the exception of the mangrove habitat surveyed in Fort Pierce. While

Clibanarius and Melongena have similar temperature and nutrient requirements, studies have demonstrated that larval Clibanarius typically require consistently

0 higher salinity (25- 30 /00) for proper development (Hathaway, 1958; Young and

Loftin, 1987; Hazlett, 1978; Lowery and Nelson, 1988; Kelly and Turner, 2011;

Garland and Kimbro, 2015). The salinity at the Cocoa site may have been high enough to support the development of Melongena but not Clibanarius. Kelly and

Turner (2011) looked at salinity levels recorded by St. John’s Water Management 47

District (SJWMD) and found that levels were below the optimal range for

Clibanarius larva for 16 out of 18 years between 1986 and 2005 at a nearby site in Cocoa. Out of the three surveys conducted in the Cocoa area by Kelly and

Turner (2011) only one Clibanarius individual was found. Salinity levels recorded by SJWMD remained below the optimum levels for Clibanarius from 2006-2015

(Personal Communication, C. Edward Proffitt). Areas such as this where

Clibanarius populations are small or absent may provide refuge for Melongena.

Shell fit was recorded for all Clibanarius individuals encountered during surveys. There was no relationship between shell fit and shell species, which indicates that, for the suite of species present in the study area, no shell species intrinsically offers a better fit than another for Clibanarius vittatus hermit crabs.

Clibanarius at the rocky site at H.B.O.I. are larger than the Clibanarius at both rocky and mangrove survey sites at Fort Pierce. As gastropods were not found at these sites, it is possible that larger shells may be more available at HBOI due to differences in currents (Vance, 1972a), predation (Pechenik and Lewis, 2000), competition (McLean, 1974; Mather, 1982) and/or shell burial rates (Reese,

1969; Kellogg, 1976). The effect of environmental factors on hermit crab behavior is not completely understood, and populations of the same species in different locations have shown wide varieties of shell-selection and preference (Kinosita &

Okajima, 1968; Elwood et. al., 1979; Hazlett 1981; Elwood & Stewart, 1985;

Hazlett, 1992; Argüelles et al., 2009). These variations could affect the sizes of individuals present.

4.4. Ecological Classification of the Interaction

Overall, this interaction does not fit into the category of either predation or competition but appears to be a unique interaction. Although the interaction results in the death of Melongena, this study clearly indicates this interaction is driven by the need for a shell (as opposed to a food source) as Clibanarius did not consume Melongena tissue at any point throughout the study. A true competition interaction is one in which both organisms have the potential to benefit. Clearly there is no benefit to Melongena for participating in this interaction. Thus, this appears to be an entirely new type of interaction requiring new terminology. I propose the term ‘lethal eviction’ for this interaction. This term denotes the fact the Clibanarius is killing Melongena in the process of separating it from its shell to obtain “protective housing” that Clibanarius requires for survival.

4.5. Future Work

While this study clearly shows that Clibanarius can obtain a shell directly from Melongena, it is unknown whether Clibanarius can obtain a shell directly from other sympatric gastropod species. Additional studies that widen the taxonomic scope to include other species of gastropods would be ecologically significant. It remains unknown how Clibanarius vittatus developed this ability while other hermit crabs have not and whether this ability is widespread.

Determining geological range of Clibanarius with this ability as well as further

elucidating the mechanistic procedure utilized by Clibanarius to maneuver under the operculum are necessary to better understand this interaction.

A greater understanding of Melongena to escape predation by Clibanarius is also necessary to understand how this interaction will affect their population sizes. Little is known about Melongena growth patterns after reaching sexual maturity. If Clibanarius typically kills Melongena shortly after they become sexually mature, populations may have difficulty successfully reproducing. On the other hand, if Clibanarius does not kill Melongena until later in its lifespan, populations of these species may be able to coexist. Additionally, it would be valuable to understand exactly which environmental parameters are necessary to provide Melongena with a place of refuge.

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