The relationship between Pagurus anachoretus and Cerithium vulgatum as affected by shell size and availability at Station de Recherches Sous-Marines et Oceanographiques in Corsica, France.

Wade Dugdale, Ryan Baker, Eleni Christoforou University of California at Santa Cruz - BIO159 - Corsica 2014

Abstract The paper expands on the hermit crab species Pagurus anachoretus and the gastropod shell Cerithium vulgatum that it inhabits. The association between claw size of P. anachoretus and C. vulgatum shell and aperture size were tested on specimens collected in situ and measured in a lab. Contrary to current literature, we found no correlation between shell and crab size with crabs from the wild. We also ran experiments in a confined tank space to test whether P. anachoretus will exchange shells for a more optimum fit, when given the opportunity. Hermit crabs, left in a tank overnight, moved into more preferable shells after empty shells were added. They arranged themselves into even more preferred shells, suggesting that they do re-sort based on shell size preference. Our results suggest that this movement occurs to improve the hermit crabs’ general fitness.

Introduction 1976; Bertness 1980), growth rate (Bertness 1980), survival and fecundity (Angel 2000). Hermit crabs, have interested biologists and As hermit crabs grow, they must find larger naturalists for centuries, dating back to shells, therefore they are frequently in the Aristotle, in 350 B. C, (translated in English search for a new shell. Hermit crabs most by D’Arcy Wentworth Thompson in 1910) often obtain shells in one of two ways. who was the first to study their nature Either directly after the snail’s death (Reese 1962). Hermit crabs (Paruroidea) following its decomposition, after the shell belong to the class called Malacostraca is deserted on the bottom’s substrate (Laidre (Aristotle 350 B. C. E), which is derived 2011) or by competition with other hermit from the Greek words ‘µαλακό’ and crabs, while most of the times both invader ‘όστρακο’ meaning soft shell. All and defender should have a benefit for the organisms’ fitness depends on resources exchange to occur (Hazlett 1981; Briffa and provided by other taxa. Hermit crabs are not Elwood 2000). A factor influening hermit an exception (Laidre 2011), relying on crabs’ fitness is that empty gastropod shells empty gastropod shells or in limited cases, are not easily found in most habitats other types of cavities (Hazlett 1981). (Childress 1972). This makes the study of Gastropod shells are of a great importance to hermit crabs and their relation to shells hermit crabs fitness, providing protection essential to ecology (Arce 2012) in order to from predation (Vance 1972). The main understand the severity of shell limitation in aspects of shells that are of interest to hermit nature (Kellogg 1976). The importance of crabs are their shape and size which hermit crabs to the environment is also influence the crab’s reproduction (Kellogg

! 1! suggested by the analysis of the 550 optimum shell in order to improve its invertebrates that live harmonically and are fitness. This prediction was supported by the dependent on hermit crabs (Williams and statement that a hermit crab that has a large McDermott 2004). Despite the limitation in choice of shells will decide on a shell closer gastropod shells, not all shells are to the optimum size, compared to a hermit appropriate (Childress 1972) for the hermit crab that has a limited amount of shells crabs, who choose shells based on their size, available (Hazlett 1992). With that said, the species (Bertness 1980; Reese 1962) i.e. following methods and results expand on shape and abundance (Reese 1962; Reese whether there is a relationship between the 1969; Bertness 1980). size of P. anachoretus and C. vulgatum and if P. anachoretus change into more optimum After observing hermit crabs at the Station shells when provided with the opportunity to de Recherches Sous-Marines et resort with other individuals in a confined Oceanographiques (STARESO), in Corsica, tank space. France, we became interested in their shell choice patterns. Therefore, our main goal was to observe, study, test and understand the relationship between the hermit crabs Materials and Methods and the shell they inhabit, in the specific Location area. We first observed that P. anachoretus has a strong preference for Cerithium The study was contacted South of vulgatum shells, which was the most STARESO field station harbor, which is abundant gastropod shell species. Hazlett located on the northwest coast of Corsica, (1981; 1992) found a strong correlation France. Fieldwork was conducted over large between the size of the shell and the size of (1-5m) sub-tidal boulders at a depth of 4- hermit crabs, and therefore we decided to 10m. The surfaces of these boulders were test it ourselves. Following the collection of primarily covered with algae and detritus. C. vulgatum shells inhabited by P. The area has very little daily tidal anachoretus, our first hypothesis was that disturbance but is affected by major storm there is a relationship between the shell size events annually. This study was conducted and the hermit crab size of these specific in October 2014 before the first major storm species in the local area. Additional event of the season. information was that, crabs in smaller than preferred shells experience a slower growth rate (Bertness 1981) and are more exposed to predation (Angel 2000; Hazlett 1981) because of their lack of space to withdraw and protect themselves. On the other hand, crabs in larger shells must carry more mass, leading to greater energy expenditure (Arce 2011). In a broader scale, a non-adequate shell negatively influences a crab’s fecundity (Vance 1972) and reduces its chance of survival (Childress 1972). Figure 1: Left: West Mediterranean with a Therefore our second hypothesis was that, in square around Corsica. Right: Corsica with a a high-density environment, P. anachoretus square around where STARESO is. (images would compete and change into a more produced by using Google maps)

! 2! Species from our study in order to prevent misrepresentation of the shell metrics.

Pagurus anachoretus is a marine decapod from the family Paguridae. This sub-tidal species ranges from 1-40 meter depth and is found throughout the Mediterranean sea. Pagurus anachoretus is omnivorous, preying primarily on tiny marine animals and opportunistically scavenging on carrion. In the study area P. anachoretus was observed to be solitary while other species of hermit crabs are known to cluster. Additionally, P. anachoretus lay and carry their eggs within the shell they inhabit.

Collections

We collected P. anachoretus individuals inhabiting C. vulgatum shells by hand using SCUBA. The collections were conducted at night given the fact that P. anachoretus are nocturnal, when the animals are more active. We collected specimens primarily from the Figure 2: The illustrations represent the tops and sides of boulders and placed them standardized linear metrics that were into sealable bags filled with seawater until initially used to measure P. anachoretus our return to the laboratory. At that time we chelae and C. vulgatum shells: chelae length measured the chelae and associated shells of (CL) and width (CW), shell length (SL), each specimen, thus minimizing the time shell width (SW) as well as the aperture availability, to ensure that no shell length (AP) and aperture width (AW) of exchanges occurred before baseline each C. vulgatum shell. measurements.

All of our measurements were taken by one Mass to Chelae Relationship technician in order to standardize the measurement data, using vernier calipers Twenty-three previously collected P. and rounding to the closest 0.5mm. We anachoretus specimens were removed from measured two linear metrics of crab size: their shells and we measured their chelae chelae length (CL) and chelae width (CW), length and width. Their mass was also to use as proxies for overall crab size measured to a thousandth of a gram. We without having to remove individuals from then ran a linear regression analysis of their shells. We measured four linear metrics bivariate fits of chelae length by crab mass of shell size: shell length (SL), shell width in order to determine whether chelae size (SW), aperture length (AL) and aperture was a viable representation of overall crab width (AW) of each shell (Figure 1). All size. This allowed us to measure the relative specimens with broken shells were excluded sizes of hermit crabs in subsequent analyses

! 3! and experiments without removing them All but 3 of the empty shells used in this from their shells. experiment were previously inhabited; we removed their inhabitants by anesthetizing them using clove oil. The reason it was Shell Crab to Shell Size Relationship necessary to use these shells was because of the lack of suitable empty shells found in the We performed a scatterplot matrix analysis local area. In the 36 hours in between the of all possible pairs between the two linear first and second trial the hermit crabs were chelae size metrics and four linear shell size kept in the same tank with constant water metrics to determine which pair of metrics flow and aeration. Small rocks and algae had the strongest correlation between crab like Padina pavonica were added to the tank and shell size. These two metrics would be for the hermit crabs to feed on. used as proxies for crab and shell size for all subsequent analyses and experiments. We ran a linear regression analysis of the best Results pair of size metrics using JMP (Statistical Discovery software for SAS) to determine Mass to Chelae relationship whether a significant relationship between chelae metrics and shell metrics existed in A regression analysis of the bivariate fit of wild hermit crabs. CL by crab mass (n=23) revealed a significant positive linear correlation between the chelae length and the mass of Shell Exchange – Trial 1 hermit crab individuals (Figure 3. F Ratio = 68.58, DF = 28, p value < .0001, R^2 = The group of specimens, from Hypothesis 1, 0.7175). The analysis indicated that there is were all placed together, immediately after a reliable relationship between chelae length measurement, in an aerated glass aquarium and crab mass. measuring 44x44x38cm with constant flowing seawater. We then covered the tank to block light and left the specimens overnight for 12 hours to competitively or cooperatively exchange shells. After the trial period, all individuals and shells (n=56) were measured again. The crab-shell size data sets from before and after the trial period were plotted using JMP and a regression line was fit to each. We then compared the F Ratios for each regression analysis in order to see the difference between the fit from the wild and the fit post trial. Figure 3: A bivariate fit of crab mass by Shell Exchange – Trial 2 chelae length.

The experiment was repeated two nights later, with the addition of 36 empty shells.

! 4! Crab to Shell Size Relationship The competitive shell exchange trials supported the hypothesis that hermit crabs Collection of hermit crabs from STARESO will exchange shells amongst each other for yielded a number of P. anachoretus more appropriately fitted shells. Regression individuals (n=56) inhabiting unbroken analyses of the bivariate fit of CL by SW Cerithium vulgatum shells that were suitable were performed using JMP before and after for study. Multiple metrics were used as each trial. The F Ratios for each set of proxies to establish the relative sizes of measurements were calculated to describe hermit crabs and shells. Two linear metrics the variance of each regression analysis. The of crab chelae size, and four linear metrics first trial, performed with wild caught crabs of shell size were recorded. A preliminary in occupied shells (n=56) and started with scatter plot matrix analysis showed that, of no significant relationship between CL and all eight possible size metric pairings that SW (Figure 4. F Ratio: 0.28, DF = 55, p could be made between crab measurements value = 0.5989, R2 = 0.0052), but ended and shell measurements, the two size with a significant positive relationship metrics with the strongest correlation for between CL and SW (Figure 5. F Ratio: relating crab size to shell size were chelae 21.05, DF = 52, p value length (CL) and shell width (SW). A = <.0001, R2 = 0.2922). regression analysis of the bivariate fit of CL by SW for each hermit crab and its associated shell (n=56) was performed to analyze the relationship between the two size metrics with individuals collected from the wild. The analysis revealed found no significant correlation between hermit crab chelae length and shell width (Figure 4. F Ratio: 0.28, DF = 55, p value = 0.5989, R2 = 0.0052).

Figure 5: A bivariate fit of CL by SW measurements taken after the completion of Shell Exchange Trial 1.

Shell Exchange - Trial 2

The bivariate fit of CL by SW in second trial (n=53) started with a significant positive linear correlation (Figure 6. F Ratio: 20.24, Figure 4: A bivariate fit of CL by SW DF = 52, p value <.0001, R2 = 0.2841) and measurements taken immediately after ended with a significant positive linear collection from the wild. correlation (Figure 7. F Ratio: 28.06, DF = Shell Exchange - Trial 1 49, p value = <.0001, R2 = 0.3689), after the

! 5! addition of 36 empty shells. The increased F crab size of different hermit crab species in Ratio indicates a stronger linear relationship other systems. As such, we observed that and lower variance after the trial. there was a significant influence affecting the shell selection of P. anachoretus in out study system. The difference in the results may be because our sample size was probably much smaller that what was used in previous studies and therefore it might lead us to erroneous conclusions. It is known that when hermit crabs encounter other individuals, they frequently exchange shells, in a cooperative or competitive manner (Hazlett 1981; Childress 1972; Briffa and Elwood 2000). Throughout our collections of hermit crabs at STARESO, only 3 suitable shells were found to be uninhabited. Figure 6: A bivariate fit of CL by SW This indicates that P. anachoretus have measurements taken before the initiation of nearly saturated the available shell resources Shell Exchange Trial 2. and are therefore primarily obtaining new shells through cooperative or competitive exchange. Our collections of individuals from the local ecosystem also highlighted the low population density of P. anachoretus, which we propose is one of the major factors inhibiting optimal shell selection. When P. anachoretus individuals were placed into an artificial environment with a high population density, we found that the hermit crabs exchanged shells in order to optimize fit, as described in other systems Figure 7: A bivariate fit of CL by SW that have been previously studied. After the measurements taken after the completion of first trial, the group of P. anachoretus that Shell Exchange Trial 2. we collected showed significant re-sorting of shells, and we established a significant positive relationship between crab size and shell size was established. Our first trial Discussion showed that P. anachoretus, like other P. anachoretus collected from the wild near species of hermit crabs, will exchange shells STARESO, Calvi Corsica did not show a with one another according to size when the significant positive relationship between opportunity arises. While our experimental their size and C. vulgatum shell size. This is design cannot elucidate whether the hermit contrary to the findings of previous studies crabs were exchanging shells cooperatively (Hazlett 1992), which suggested strong or competitively, this trial suggests that correlations between the shell and hermit population density influences shell exchange, via the mechanism of individual

! 6! encounters, and supports the idea that the structure might have a larger effect upon the low population density of P. anachoretus shells that the hermit crabs inhabit, than the observed at STARESO is one of the factors characteristics of the shells themselves. inhibiting size-based shell selection in the wild. In the environment near STARESO, suitable Recommendations for future studies shells are a limiting resource for P. While performing our experiments and anachoretus; it is unlikely that there will be analyzing our results, some questions and more hermit crab individuals than there are ideas came to mind for potential future available shells at any given time. Our studies. Some of the hermit crabs that were second trial showed that, after pulled out of their shells (Mass to Chelae cooperative/competitive sorting and a Relationship) were carrying eggs. That significant positive relationship between might suggest a difference between the size crab size and shell size, the addition of of shell a female P. anachoretus would empty shells allowed the crabs to further choose, making sure that there is enough refine their shell selection based on relative space for her eggs to develop, in comparison size. The empty shells allowed crabs to swap to a male P. anachoretus. for more optimal shells. The number of empty shells added (n=36) was not the same An interesting observation was made during as the number of crab individuals in the trial the preliminary research period, our first (n=53), which may have even prevented experimental design involved placing hermit further optimization of fit, but this crabs in individual mini tanks and offering experiment was limited by the low number them shells to observe if they would take of empty C. vulgatum shells available. This shells of a better fit. This experiment did not dynamic showed that not only is optimal yield conclusive results, as many of the shell selection inhibited by the low specimens died during the trial and others population density of P. anachoretus but crawled out of their shells. We believe that also that the low availability of shells may this is related to the lack of oxygen in the be limiting the size of the population present mini tanks. Since P. anachoretus is a sub- near STARESO. Both of these factors may tidal species we believe that is not as negatively affect the fitness of P. adapted to low oxygen environments as anachoretus individuals by making it other tidal species of hermit crabs. It may be difficult for them to find protection against interesting to test for low oxygen tolerance predation or find a mate for reproduction in P. anachoretus. purposes. While diving in this area we observed 3 In summary, this study explored the other species of hermit crabs. Of the four characteristics driving shell exchange in P. species P. anachoretus was by far the most anachoretus near STARESO. We were numerous. We also observed at least two surprised to find little evidence of size based other types of shells inhabited by all 4 shell selection in wild populations, but our species. This made us wonder whether P. experimental trials aimed to separate the anachoretus really prefer C. vulgatum shells mechanisms preventing shell selection in the or if the other species are competitively local population. We discovered that when excluding them from the other shells or shells are limiting, the ecological could we be seeing niche partitioning in this characteristics of the hermit crab population system? We believe this would be an

! 7! interesting question to address in future clutch size. Crustaceana 40(2): 197– studies. 205 Briffa, M., and R. W Elwood.(2000) The Power of Shell Rapping Influences Acknowledgments Rates of Eviction in Hermit Crabs. We would like to thank Pete Raimondi and Behavioral Ecology 11(3): 288-93. Giacomo Bernardi as without their help this Web. 14 Dec. 2014. research and paper would not have been Childress, J.R. 1972. Behavioral ecology possible. We also want to thank Colin and fitness theory in a tropical hermit Gaylord, Gary Longo, Easton Williams, crab Ecology. 53: 960–964 Daniel O’Shea, Shohei Burns, Kenan Chan, Adri Sparks and Lora Johansen for their Hazlett, B.A. 1981. The behavioral ecology help in collecting the specimens and the of hermit crabs. Ann. Rev. Ecol. recording of the measurements. Special Syst. 12:1–22 thanks go to Gary Longo and Louis Hadjioannou for the proofreading of our Hazlett, B.A. 1992. The Effect of past final draft. Additionally we thank Kate Experience on the Size of Shells Melanson, Kristy Kroeker, STARESO staff Selected by Hermit Crabs. Animal and all our classmates in Corsica 2014. Behaviour 44(2): 203-05. Web. 28 Nov. 2014.

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! 8! worldwide review of the diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 305: 1-128.

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