The relationship between Pagurus anachoretus and Cerithium vulgatum
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1 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 Hermit crabs, have interested biologists and naturalists for centuries, dating back to Aristotle, in 350 B. C, (translated in English by D Arcy Wentworth Thompson in 1910) who was the first to study their nature (Reese 1962). Hermit crabs (Paruroidea) belong to the class called Malacostraca (Aristotle 350 B. C. E), which is derived from the Greek words µαλακό and όστρακο meaning soft shell. All organisms fitness depends on resources provided by other taxa. Hermit crabs are not an exception (Laidre 2011), relying on empty gastropod shells or in limited cases, other types of cavities (Hazlett 1981). Gastropod shells are of a great importance to hermit crabs fitness, providing protection from predation (Vance 1972). The main aspects of shells that are of interest to hermit crabs are their shape and size which influence the crab s reproduction (Kellogg 1976; Bertness 1980), growth rate (Bertness 1980), survival and fecundity (Angel 2000). As hermit crabs grow, they must find larger shells, therefore they are frequently in the search for a new shell. Hermit crabs most often obtain shells in one of two ways. Either directly after the snail s death following its decomposition, after the shell is deserted on the bottom s substrate (Laidre 2011) or by competition with other hermit crabs, while most of the times both invader and defender should have a benefit for the exchange to occur (Hazlett 1981; Briffa and Elwood 2000). A factor influening hermit crabs fitness is that empty gastropod shells are not easily found in most habitats (Childress 1972). This makes the study of hermit crabs and their relation to shells essential to ecology (Arce 2012) in order to understand the severity of shell limitation in nature (Kellogg 1976). The importance of hermit crabs to the environment is also! 1
2 suggested by the analysis of the 550 invertebrates that live harmonically and are dependent on hermit crabs (Williams and McDermott 2004). Despite the limitation in gastropod shells, not all shells are appropriate (Childress 1972) for the hermit crabs, who choose shells based on their size, species (Bertness 1980; Reese 1962) i.e. shape and abundance (Reese 1962; Reese 1969; Bertness 1980). After observing hermit crabs at the Station de Recherches Sous-Marines et Oceanographiques (STARESO), in Corsica, 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 and the shell they inhabit, in the specific area. We first observed that P. anachoretus has a strong preference for Cerithium vulgatum shells, which was the most abundant gastropod shell species. Hazlett (1981; 1992) found a strong correlation between the size of the shell and the size of hermit crabs, and therefore we decided to test it ourselves. Following the collection of C. vulgatum shells inhabited by P. anachoretus, our first hypothesis was that there is a relationship between the shell size and the hermit crab size of these specific species in the local area. Additional 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). Therefore our second hypothesis was that, in a high-density environment, P. anachoretus would compete and change into a more optimum shell in order to improve its fitness. This prediction was supported by the statement that a hermit crab that has a large choice of shells will decide on a shell closer to the optimum size, compared to a hermit crab that has a limited amount of shells available (Hazlett 1992). With that said, the following methods and results expand on whether there is a relationship between the size of P. anachoretus and C. vulgatum and if P. anachoretus change into more optimum shells when provided with the opportunity to resort with other individuals in a confined tank space. Materials and Methods Location The study was contacted South of STARESO field station harbor, which is located on the northwest coast of Corsica, France. Fieldwork was conducted over large (1-5m) sub-tidal boulders at a depth of 4-10m. The surfaces of these boulders were primarily covered with algae and detritus. The area has very little daily tidal disturbance but is affected by major storm events annually. This study was conducted in October 2014 before the first major storm event of the season. Figure 1: Left: West Mediterranean with a square around Corsica. Right: Corsica with a square around where STARESO is. (images produced by using Google maps)! 2
3 Species 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. from our study in order to prevent misrepresentation of the shell metrics. 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 tops and sides of boulders and placed them into sealable bags filled with seawater until our return to the laboratory. At that time we measured the chelae and associated shells of each specimen, thus minimizing the time availability, to ensure that no shell exchanges occurred before baseline measurements. All of our measurements were taken by one technician in order to standardize the measurement data, using vernier calipers and rounding to the closest 0.5mm. We measured two linear metrics of crab size: chelae length (CL) and chelae width (CW), to use as proxies for overall crab size without having to remove individuals from their shells. We measured four linear metrics of shell size: shell length (SL), shell width (SW), aperture length (AL) and aperture width (AW) of each shell (Figure 1). All specimens with broken shells were excluded Figure 2: The illustrations represent the standardized linear metrics that were initially used to measure P. anachoretus chelae and C. vulgatum shells: chelae length (CL) and width (CW), shell length (SL), shell width (SW) as well as the aperture length (AP) and aperture width (AW) of each C. vulgatum shell. Mass to Chelae Relationship Twenty-three previously collected P. anachoretus specimens were removed from their shells and we measured their chelae length and width. Their mass was also measured to a thousandth of a gram. We then ran a linear regression analysis of bivariate fits of chelae length by crab mass in order to determine whether chelae size was a viable representation of overall crab size. This allowed us to measure the relative sizes of hermit crabs in subsequent analyses! 3
4 and experiments without removing them from their shells. Shell Crab to Shell Size Relationship We performed a scatterplot matrix analysis of all possible pairs between the two linear chelae size metrics and four linear shell size metrics to determine which pair of metrics had the strongest correlation between crab and shell size. These two metrics would be used as proxies for crab and shell size for all subsequent analyses and experiments. We ran a linear regression analysis of the best pair of size metrics using JMP (Statistical Discovery software for SAS) to determine whether a significant relationship between chelae metrics and shell metrics existed in wild hermit crabs. Shell Exchange Trial 1 The group of specimens, from Hypothesis 1, were all placed together, immediately after measurement, in an aerated glass aquarium 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. Shell Exchange Trial 2 All but 3 of the empty shells used in this experiment were previously inhabited; we removed their inhabitants by anesthetizing them using clove oil. The reason it was necessary to use these shells was because of the lack of suitable empty shells found in the local area. In the 36 hours in between the first and second trial the hermit crabs were kept in the same tank with constant water flow and aeration. Small rocks and algae like Padina pavonica were added to the tank for the hermit crabs to feed on. Results Mass to Chelae relationship A regression analysis of the bivariate fit of CL by crab mass (n=23) revealed a significant positive linear correlation between the chelae length and the mass of hermit crab individuals (Figure 3. F Ratio = 68.58, DF = 28, p value <.0001, R^2 = ). The analysis indicated that there is a reliable relationship between chelae length and crab mass. Figure 3: A bivariate fit of crab mass by chelae length. The experiment was repeated two nights later, with the addition of 36 empty shells.! 4
5 Crab to Shell Size Relationship Collection of hermit crabs from STARESO yielded a number of P. anachoretus individuals (n=56) inhabiting unbroken Cerithium vulgatum shells that were suitable for study. Multiple metrics were used as proxies to establish the relative sizes of hermit crabs and shells. Two linear metrics of crab chelae size, and four linear metrics of shell size were recorded. A preliminary scatter plot matrix analysis showed that, of all eight possible size metric pairings that could be made between crab measurements and shell measurements, the two size metrics with the strongest correlation for relating crab size to shell size were chelae length (CL) and shell width (SW). A 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 = , R 2 = ). The competitive shell exchange trials supported the hypothesis that hermit crabs will exchange shells amongst each other for more appropriately fitted shells. Regression analyses of the bivariate fit of CL by SW were performed using JMP before and after each trial. The F Ratios for each set of measurements were calculated to describe the variance of each regression analysis. The first trial, performed with wild caught crabs in occupied shells (n=56) and started with no significant relationship between CL and SW (Figure 4. F Ratio: 0.28, DF = 55, p value = , R 2 = ), but ended with a significant positive relationship between CL and SW (Figure 5. F Ratio: 21.05, DF = 52, p value = <.0001, R 2 = ). Figure 5: A bivariate fit of CL by SW measurements taken after the completion of Shell Exchange Trial 1. Shell Exchange - Trial 2 Figure 4: A bivariate fit of CL by SW measurements taken immediately after collection from the wild. Shell Exchange - Trial 1 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, DF = 52, p value <.0001, R 2 = ) and ended with a significant positive linear correlation (Figure 7. F Ratio: 28.06, DF = 49, p value = <.0001, R 2 = ), after the! 5
6 addition of 36 empty shells. The increased F Ratio indicates a stronger linear relationship and lower variance after the trial. Figure 6: A bivariate fit of CL by SW measurements taken before the initiation of Shell Exchange Trial 2. Figure 7: A bivariate fit of CL by SW measurements taken after the completion of Shell Exchange Trial 2. Discussion P. anachoretus collected from the wild near STARESO, Calvi Corsica did not show a significant positive relationship between their size and C. vulgatum shell size. This is contrary to the findings of previous studies (Hazlett 1992), which suggested strong correlations between the shell and hermit crab size of different hermit crab species in other systems. As such, we observed that 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. This indicates that P. anachoretus have nearly saturated the available shell resources 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 that have been previously studied. After the first trial, the group of P. anachoretus that 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 showed that P. anachoretus, like other species of hermit crabs, will exchange shells with one another according to size when the opportunity arises. While our experimental design cannot elucidate whether the hermit crabs were exchanging shells cooperatively or competitively, this trial suggests that population density influences shell exchange, via the mechanism of individual! 6
7 encounters, and supports the idea that the low population density of P. anachoretus observed at STARESO is one of the factors inhibiting size-based shell selection in the wild. In the environment near STARESO, suitable shells are a limiting resource for P. anachoretus; it is unlikely that there will be more hermit crab individuals than there are available shells at any given time. Our second trial showed that, after cooperative/competitive sorting and a significant positive relationship between crab size and shell size, the addition of empty shells allowed the crabs to further refine their shell selection based on relative size. The empty shells allowed crabs to swap for more optimal shells. The number of empty shells added (n=36) was not the same as the number of crab individuals in the trial (n=53), which may have even prevented further optimization of fit, but this experiment was limited by the low number of empty C. vulgatum shells available. This dynamic showed that not only is optimal shell selection inhibited by the low population density of P. anachoretus but also that the low availability of shells may be limiting the size of the population present near STARESO. Both of these factors may negatively affect the fitness of P. anachoretus individuals by making it difficult for them to find protection against predation or find a mate for reproduction purposes. In summary, this study explored the characteristics driving shell exchange in P. anachoretus near STARESO. We were surprised to find little evidence of size based shell selection in wild populations, but our experimental trials aimed to separate the mechanisms preventing shell selection in the local population. We discovered that when shells are limiting, the ecological characteristics of the hermit crab population structure might have a larger effect upon the shells that the hermit crabs inhabit, than the characteristics of the shells themselves. Recommendations for future studies While performing our experiments and analyzing our results, some questions and ideas came to mind for potential future studies. Some of the hermit crabs that were pulled out of their shells (Mass to Chelae Relationship) were carrying eggs. That might suggest a difference between the size of shell a female P. anachoretus would choose, making sure that there is enough space for her eggs to develop, in comparison to a male P. anachoretus. An interesting observation was made during the preliminary research period, our first experimental design involved placing hermit crabs in individual mini tanks and offering them shells to observe if they would take shells of a better fit. This experiment did not yield conclusive results, as many of the specimens died during the trial and others crawled out of their shells. We believe that this is related to the lack of oxygen in the mini tanks. Since P. anachoretus is a subtidal species we believe that is not as adapted to low oxygen environments as other tidal species of hermit crabs. It may be interesting to test for low oxygen tolerance in P. anachoretus. While diving in this area we observed 3 other species of hermit crabs. Of the four species P. anachoretus was by far the most numerous. We also observed at least two other types of shells inhabited by all 4 species. This made us wonder whether P. anachoretus really prefer C. vulgatum shells or if the other species are competitively excluding them from the other shells or could we be seeing niche partitioning in this system? We believe this would be an! 7
8 interesting question to address in future studies. Acknowledgments We would like to thank Pete Raimondi and Giacomo Bernardi as without their help this research and paper would not have been possible. We also want to thank Colin Gaylord, Gary Longo, Easton Williams, Daniel O Shea, Shohei Burns, Kenan Chan, Adri Sparks and Lora Johansen for their help in collecting the specimens and the recording of the measurements. Special thanks go to Gary Longo and Louis Hadjioannou for the proofreading of our final draft. Additionally we thank Kate Melanson, Kristy Kroeker, STARESO staff and all our classmates in Corsica References Angel, J.E Effects of shell fit on the biology of the hermit crab Pagurus longicarpus (Say). J. Exp Mar. Biol. Ecol. 243: Arce, E. and G. Alcaraz Shell use by the hermit crab Calcinus californiensis at different levels of the intertidal zone. Sci Mar 75: Arce, E. and G. Alcaraz. Shell Preference in a Hermit Crab: comparison between a Matrix of Paired Comparisons and a Multiple-alternative Experiment. 159(4): Web. 25 Nov Bertness, M.D Shell preference and utilization patterns in littoral hermit crabs of the bay of Panama. J. Exp. Mar. Biol. Ecol. 48:1 16. Bertness, M.D The influence of shelltype on hermit crab growth rate and clutch size. Crustaceana 40(2): Briffa, M., and R. W Elwood.(2000) The Power of Shell Rapping Influences Rates of Eviction in Hermit Crabs. Behavioral Ecology 11(3): Web. 14 Dec Childress, J.R Behavioral ecology and fitness theory in a tropical hermit crab Ecology. 53: Hazlett, B.A The behavioral ecology of hermit crabs. Ann. Rev. Ecol. Syst. 12:1 22 Hazlett, B.A The Effect of past Experience on the Size of Shells Selected by Hermit Crabs. Animal Behaviour 44(2): Web. 28 Nov Kellogg, C.W Gastropod shells: a potentially limiting resource for hermit crabs. J. Exp. Mar. Biol. Ecol. 22: Laidre, M.E Ecological Relations between Hermit Crabs and Their Shell-supplying Gastropods: Constrained Consumers. J. Exp. M. Biol. Ecol. 397(1): Web. 28 Nov Reese, E.S Shell Selection Behaviour of Hermit Crabs. Animal Behaviour 10(3-4): Web. 28 Nov Reese, E.S Behavioral adaptations of intertidal hermit crabs Am. Zool., 9(2): Vance, R.R The role of shell adequacy in behavior interactions involving hermit crabs. Ecology. 53: Williams J.D and McDermott J Hermit crab biocoenoses: a! 8
9 worldwide review of the diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 305: ! 9
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