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Group size and individual ‘personality’ influence emergence times in hermit crabs

Group size and individual ‘personality’ influence emergence times in hermit crabs Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 BioscienceHorizons Volume 00 2018 10.1093/biohorizons/hzy011 ............................................................................................ ..................................................................... Research article Group size and individual ‘personality’ influence emergence times in hermit crabs Harvey Eliot Broadhurst and Lesley J. Morrell School of Environmental Sciences, University of Hull, Yorkshire, HU6 7RX, UK *Corresponding author: Harvey Eliot Broadhurst, Email: harv.broadhurst@gmail.com Supervisor: Lesley J. Morrell, School of Environmental Sciences (Biology), Hardy Building, University of Hull, Kingston-upon-Hull HU6 7RX. ............................................................................................ ..................................................................... Many animals benefit from aggregating due to the anti-predator effects associated with living in groups. Hermit crabs are known to form groups, or ‘clusters’, which may occur at sites of high shell availability. Clustering may also have anti-predator benefits, if individuals in larger clusters able to spend less time engaging in defensive behaviours such as hiding in their shells. Here, we test the hypothesis that crabs in larger clusters will emerge faster from their shells after an elicited startle response in the European hermit crab (Pagurus bernhardus). We found that individuals were generally consistent in their emergence times across group sizes (displaying ‘personality’ in relation to emergence time), but that group size influenced emergence time in P. bernhardus. In contrast to the hypothesis, crabs in larger clusters had longer emergence times relative to their own emergence times in smaller clusters. Suggested explanations for this effect include intra-specific competition for the gastropod shells that hermit crabs inhabit, as well as the possible release of chemical cues by crabs in larger clusters. Key words: hermit crabs, emergence time, personality, group size, behavioural consistency, Pagurus bernhardus Submitted on 3 March 2017; editorial decision on 29 October 2018 ............................................................................................ ..................................................................... in other activities (Pulliam, 1973; Cresswell and Quinn, Introduction 2011), which can also allow for cooperative warning, escape and defence behaviour (Krause and Ruxton, 2002). However, Group-living has been observed across a broad range of ani- as group size increases, individuals may also be subjected to mal taxa (Krause and Ruxton, 2002), and group size in par- increased competition for resources, which could be a limiting ticular has a major influence on the outcome of predator–prey factor in group size regulation (Grand and Dill, 1999). interactions, allowing group-living animals to manage their vulnerability to predation risk (Cresswell and Quinn, 2011). ‘Clustering’ has been identified as a behavioural strategy in The major costs associated with group-living, such as higher several hermit crab (superfamily Paguroidea) species, (Taylor, rate of attack from predators due to increased conspicuous- 1981; Gherardi and Vannini, 1989). Hermit crabs aggregate at ness, may be offset by anti-predator mechanisms (Uetz et al., sites of gastropod mortality, possibly to engage in ‘vacancy 2002). These mechanisms include the dilution of individual chain’ behaviour; the sequential distribution of the acquired risk (Foster and Treherne, 1981), the confusion of predators, gastropod shells that hermit crabs inhabit (Lewis and Rotjan, reducing attack success (Miller, 1922; Krakauer, 1995), 2009). When a hermit crab vacates its shell in order to occupy encounter-dilution (Turner and Pitcher, 1986) and selfish amore suitableone, other crabs have beenobserved ‘lining up’ herd effects (Hamilton, 1971). Grouping individuals also in order to vacate their own shells in favour of a newly avail- benefit from collective vigilance, with those in larger groups able one (De Waal, 2005). In P. bernhardus, the structure of able to reduce time spent scanning and increase time engaging these vacancy chains differs in the presence and absence of ............................................................................................... .................................................................. © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. predation risk (Briffa and Austin, 2009), but it is not known This study investigates whether P. bernhardus exhibits reac- whether the size of a cluster affects predation risk. Hermit tion norm variation across individuals when exposed to differ- crabs in the genus Pagurus do exhibit alarm responses when ent degrees of clustering (i.e. different group sizes). By exposed to the chemical cue of a crushed conspecific(Rittschof analyzing the variation in startle responses exhibited by indi- et al.,1992), and therefore clustering may serve an anti- vidual hermit crabs across several classes of group size, this predator function, with individuals benefiting from dilution or study explores whether emergence time is influenced by cluster- detection effects. However, larger clusters may also carry ing in P. bernhardus. If cluster size in this species is influenced increased risk of competition for shells from conspecifics. by both the anti-predator benefits and competition-associated costs of group-living, we expect to find a significant effect of Hermit crabs employ two major defences when exposed to group size on emergence time. If this species forms clusters as a potential predation: fleeing and refuging within their acquired response to predation risk, or gains anti-predator benefits from gastropod shells (Scarratt and Godin, 1992). If, on detecting a clustering, individuals are predicted to register shorter emer- predator, a crab decides to hide within the shell, then there is gence times in larger groups (where individual risk is lower) an associated second decision that determines the length of relative to their emergence times in smaller groups (where indi- time wherein the crab will remain hidden before emerging vidual risk is higher). Alternatively, if clustering carries once again (Briffa and Twyman, 2011). This decision to increased risk of competition, we might expect individuals in emerge is sensitive to the perceived risk of predation (Scarratt larger groups to remain in their shells for longer periods, to and Godin, 1992). For example, the presence of chemical reduce the risk of engaging in shell fights. Additionally, we pre- cues in the form of effluent from the predatory rock crab, dict that individual hermit crabs show significant patterns of Cancer productus, has been shown to significantly reduce individual consistency across different group sizes. emergence times in hermit crabs; whereas exposure to effluent from the herbivorous kelp crab, Pugettia productus, showed no difference from a saltwater control (Rosen, Schwarz and Methods Palmer, 2009). Withdrawal into a shell is also a response to competition: individuals are able to defend themselves from Data collection competitors in shell fights by retreating into their shells to avoid being forcibly removed (Courtene-Jones and Briffa, Sixty Pagurus bernhardus were collected from South Bay, 2014), and thus the decision to emerge may also be sensitive Scarborough, UK (54°16′12″N0°23′25″W) in October 2015. to the risk of competition. Emergence from a startle is also They were transported back to the laboratory at the consistent across individuals, with some showing consistently University of Hull within 4 h of collection, where they were longer recovery times, while others show consistently shorter kept in a holding tank (1.5-m circular diameter) that con- times (Briffa, Rundle and Fryer, 2008; Briffa and Twyman, tained steadily filtered aerated saltwater at a constant tem- 2011; Briffa, Bridger and Biro, 2013; Briffa, 2013). perature of 11°C. Crabs were given access to a large number of vacant shells of varying size (primarily common periwin- Rather than responding optimally across every situation kle, Littorina littorea; dog whelk, Nucella lapillus; and flat (behavioural plasticity), some individuals are constrained by top shell, Gibbula umbilicalis) and left to acclimatize to their consistent differences in behaviour over time or across con- new surroundings (and occupy a new shell if required) for texts (sometimes known as ‘animal personality’; Mathot and 72 h. Following acclimatization, 25 crabs were randomly Dingemanse, 2014). Startle responses may therefore be con- selected, weighed within their shells and individually num- sistent between individuals, forming a component of a ‘behav- bered on the shell using nail varnish, then placed inside plastic ioural syndrome’; which occurs when behaviours are containers (18 × 10 cm; one side meshed for aeration) within correlated across multiple behavioural categories (Jandt et al. the holding tank to isolate them and prevent shell-swapping 2014). One behaviour which is often reported as consistent is (Gherardi, 2006), a behaviour observed in the holding tank the ‘shyness-boldness’ axis, allowing for the classification of among unmarked individuals. Crabs were fed twice a week individuals as somewhere between ‘shy’ or ‘bold’ (Wilson on chopped mussel purchased from a local supermarket. et al., 1994). A bold individual would emerge rapidly from a Crabs were not sexed as previous studies have found that startle stimulus, while a shy would not (Briffa, Rundle and individual differences in startle response are independent of Fryer, 2008), and in P. bernhardus is correlated with each sex (Briffa, Rundle and Fryer, 2008). individual’s willingness to engage in ‘risky’ behaviour (Gherardi, Aquiloni and Tricarico, 2012). Behaviour however Startle response times for each marked individual were is also plastic in response to environmental conditions, and measured in five different group sizes (1, 2, 5, 10 and 20 indi- individuals can adapt their behaviour to the environment viduals). A group consisted of the marked individual and an (Pigliucci, 2001). In P. bernhardus, this plasticity is exceeded appropriate number of unmarked specimens selected haphaz- by individual consistency in boldness in response to high- and ardly from the holding tank. A circular observation container low-predation risk scenarios (Briffa, Rundle and Fryer, (35 cm diameter) was filled to a depth of 10 cm with water 2008). These between-individual differences over an environ- taken from the holding tank. The focal crab and the correct mental gradient (context) are termed ‘behavioural reaction number of unmarked individuals were placed onto a plate norms’ (Briffa, Bridger and Biro, 2013). (22 cm diameter), ensuring that the focal crab was positioned ............................................................................................... .................................................................. 2 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. in an inverted position to ensure it withdrew fully into its shell comparisons with all reference levels can be found in before observations began. All crabs were then gently tipped Appendix I). Body size was included as an additional fixed into the observation container. This method of eliciting a star- effect, and the identity of the crab was included as a random tle response is both successful and non-harmful in determin- effect to account for multiple measures on each individual ing response times of P. bernhardus (Briffa, Rundle and both within and between group sizes. Data were log- Fryer, 2008; Briffa, 2013). transformed to meet the assumptions of normality for statis- tical analysis, and non-significant interactions between body Latency to emerge from the shell was timed to the nearest size and group size were removed. second using a digital stopwatch from the point that the crab enters the observation container until the point at which its To investigate whether different individuals had predict- pereopods made contact with the base of the container ably different emergence times, an ANCOVA model was used (Briffa, 2013), when it is considered to be fully emerged. After on data from across all group sizes. This included the emer- emergence, the focal crab was returned to its individual con- gence time of the crab as the independent variable, the crab’s tainer, and the remaining crabs to the holding tank. The water identity as a dependent variable, and the group size that the in the observation container was changed between each trial. emergence time was obtained from as a covariate. A series of Each crab was given a maximum of 3 min to emerge before regression analyses were then used to further assess whether the trial was terminated (failure to emerge was recorded in an individual’s emergence time in one group size was a signifi- 61/375 trials). Startle responses were induced in each crab cant predictor of their respective emergence time in another twice a week for seven and a half weeks with each crab pro- group size. A total of 10 linear regressions were used in this viding up to 15 latencies in total, with 3 at each of the 5 group manner, with the mean emergence time of each crab in a given sizes to evaluate consistency of emergence time within a con- group size being regressed against their mean emergence time text (group size). Crabs were assigned a group size at random in another group size, until each group size had been com- during each data collection session, while ensuring that each pared against every other condition. To quantify individual experienced each group size a maximum of three times. consistency, repeatability was calculated using the intraclass correlation coefficient (r ); a measure of test–retest reliability IC Ethical approval was obtained from the School and (Uher, 2011). This was achieved using the R package ‘ICC’ Faculty Ethics Committees before the study began. At the end (Wolak, Fairbairn and Paulsen, 2012). of the experiment, the crabs were returned to the shore where they were collected from. Results Statistical analyses Does group size affect emergence time? To assess the relationship between group size and the time Accounting for individual variation in startle response, emer- that it took individuals to emerge from their shells, linear gence time increased with group size (Table 1, Fig. 1). There mixed-effects models were implemented using the package was no significant effect of body size on emergence time ‘nlme’ (Pinheiro et al., 2015) in R version 3.2.3 (R Core (Table 1). Treatment groups were compared against a group Team, 2015). Since the nature of the data involved several size of 2 as this was the group with the lowest mean emer- group size classes (1, 2, 5, 10 and 20), group size was treated gence time (Fig. 2). Crabs emerged faster in groups of 10 and as a categorical variable during analysis. Group sizes were 20 than they did in groups of 2 (Table 1). All other pairwise compared to a reference level of group size 2, as this was the comparisons can be found in Appendix I. group size with the lowest mean emergence time (pairwise Table 1. Linear mixed-effects models assessing the relationship between group size, body size and emergence time with individual identity as a random effect. Significant P-values are highlighted in bold. Value SE df tP Group size as a categorical variable (intercept: group size = 2) (intercept) 2.150 0.493 285 Group size = 1 0.225 0.161 285 1.391 0.165 Group size = 5 0.231 0.158 285 1.456 0.147 Group size = 10 0.400 0.160 285 2.492 0.013 Group size = 20 0.426 0.164 285 2.595 0.010 Body size 0.156 0.120 23 1.309 0.234 ............................................................................................... .................................................................. 3 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. consistently emerging rapidly from their shells, while those with longer emergence time (‘shy’ individuals) having consist- ently longer emergence times. The positive relationship between larger group size and longer emergence times suggest that competition with conspecifics, rather than the anti- predator benefits of grouping, are the key determinant of emergence decisions. Two related factors may explain this relationship: direct competition for gastropod shells and exposure to ‘fighting cues’ from conspecifics. Competition for gastropod shells is well-documented in hermit crabs (Elwood and Glass, 1981; Briffa, Elwood and Dick, 1998; Caven, Clayton and Sweet, 2012). Increased emergence times in larger groups may be explained by unin- tentional interference between individuals as they begin to move and emerge, such as shell-to-shell hitting or knocking. This type of disturbance would cause an emerging crab to retreat into their shell (Edmonds and Briffa, 2016), regardless of group size, but is probabilistically more likely as group size, and therefore density, increased. A tap to the shell during emergence could indicate to the crab that the risk of competi- tion was high, as it may be able to perceive whether the source of the tap was initiating a fight or not, and, given that crabs Figure 1. Bar graph showing mean responses of all crabs across group were likely to be in preferred-size shells, would have with- sizes with standard error represented as error bars. Significant effects drawn into the shell in defence (Elwood and Glass, 1981). of group size on emergence time are shown between a group size of 2 and 10, and 2 and 20. Any anti-predator benefits potentially gained from cluster- ing may have been offset by the risk of forced shell-eviction Do hermit crabs exhibit personality? from a conspecific. Indeed, in the wild, many members of the genus Pagurus are known to maintain a ‘rather large individ- Emergence times differed between crabs, even when account- ual distance’ instead of aggregating (Hazlett, 1968). Shell ing for variation caused by the different group sizes (group fights are often initiated by larger crabs and crabs that occupy size effect, F = 4.28, df = 1288, P = 0.03; individual effect, poor quality and/or unsuitably small shells (Dowds and F = 5.67, df = 24 288, P < 0.001; Fig. 3). In 8 out of 10 group Elwood, 1985), although we found no effect of size on emer- size comparisons, the emergence time registered by a crab in gence time. As crabs in this study were able to select from one group was found to be a significant predictor of how that unoccupied shells before experiments began, they may have crab would respond in other group sizes (Fig. 2; Table 2); this had low motivation to initiate a fight and maximal motivation shows consistency in the behaviour of crabs between treat- to retain their shells. As potential competition increases ments. No significant correlation was observed between emer- (increasing numbers of nearby conspecifics) motivation to gence times in group sizes of 1 and 10 (t = 1.67, P = 0.11), remain in the shell, defending it against competitions, may and 5 and 20 (t = 1.86, P = 0.08). have increased, as ‘shy’ behaviour is associated with higher Across all groups, emergence time was found to be gener- chances of successful shell-defence during a fight (Courtene- ally repeatable when measured with the intraclass correlation Jones and Briffa, 2014). As motivation to fight in hermit crabs coefficient (r = 0.26; Fig. 4). However, considering each is dependent on the quality of their shells (Elwood and Briffa, IC group size alone, significant repeatability was only found in a 2001), future studies may therefore benefit from examining group size of 2 (r = 0.56) and a group size of 20 (r = how individual emergence behaviour varies when crabs are IC IC 0.51). All other treatment groups returned an r value which housed in shells of varying size, quality and fit. IC had a 95% confidence interval inclusive of zero (Fig. 4), indic- Hermit crabs are also able to use chemical cues in order to ating non-significant repeatability despite the overall result. detect conspecifics and discriminate shells (Benoit, Peeke and Chang, 1997), and to distinguish between crabs that have recently fought and crabs that have not (Briffa and Williams, Discussion 2006). Exposure to these ‘fighting cues’ lengthens the amount of time a hermit crab spends withdrawn into its shell (Briffa The results suggest that both individual consistency and and Williams, 2006). Therefore, if the unmarked crabs had group size affect emergence time in hermit crabs. Individual been engaged in fights, the presence of fighting cues in the crabs were consistent in their behaviour across group sizes: water may have increased time spent withdrawn in the shell those with shorter emergence times (‘bolder’ individuals) ............................................................................................... .................................................................. 4 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. Figure 2. Significant positive correlations between crab emergence times in two group sizes; one larger than the other. Significance in these regressions represents predictability of an individual’s behaviour across treatments. Each data point represents an individual crab’s mean log emergence time at the specified group size. Group sizes are indicated on the axes of the graphs. in larger groups, where the probability of any one crab having The degree in which hermit crabs are able to detect discrete recently engaged in a fight would be increased, particularly as differences in conspecific group size is not known, forming a crowding is associated with increased aggression (Hazlett, potentially enlightening area for future investigation. The sug- 1968). In the green swordtail (Xiphophorus helleri), ‘eaves- gestion that animals are able to discriminate quantity through dropping’ on fights reduces a bystander’s propensity to the mental representation of numbers (counting)—as opposed engage in aggressive behaviour with the winning combatant to through non-numerical perceptible variables which differ post-fight (Earley and Dugatkin, 2002). with numerosity—has traditionally been restricted to mammalian ............................................................................................... .................................................................. 5 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. Figure 3. Box and whisker diagrams for each crab showing variation in emergence time across all treatments. Grey box represents interquartile range with black line representing the median emergence time; outliers are represented as grey circles. Table 2. Pairwise comparisons of emergence time in five different group sizes. Significance (indicated by bold) represents predictability of an individual’s behaviour across treatments. Group size comparison tP n R 1 and 2 2.16 0.04 24 0.18 1 and 5 2.66 0.01 25 0.26 1 and 10 1.67 0.11 25 0.11 1 and 20 2.31 0.03 25 0.19 2 and 5 2.75 0.01 24 0.26 2 and 10 3.36 <0.01 24 0.34 2 and 20 3.05 <0.01 24 0.30 5 and 10 2.27 0.03 25 0.18 5 and 20 1.86 0.08 25 0.13 10 and 20 2.71 0.01 25 0.24 Figure 4. Intraclass correlation coefficients for all treatments and each group size separately, represented by data points and lines indicating the 95% confidence intervals. Grey dashed line represents zero. r IC models (Agrillo et al., 2009). However, previous studies have values with intervals not crossing zero are considered significant (black documented counting of conspecifics in mosquitofish data points and lines) whereas intervals crossing zero are considered (Gambusia holbrooki; Agrillo et al., 2008), as well as the non-significant (grey data points and lines). counting of landmarks in honey bees (Apis mellifera; Chittka and Geiger, 1995). The relationship between group size and emergence time discovered in this study therefore presents a In line with previous work (Briffa, Rundle and Fryer, 2008; novel opportunity to explore quantity discrimination in a Briffa and Twyman, 2011; Briffa, Bridger and Biro, 2013; Briffa, crustacean model. 2013), hermit crabs showed significant individual consistency in ............................................................................................... .................................................................. 6 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. behaviour across group sizes, yet adjusted that behaviour in transportation of the hermit crabs that this project required, response to their environment. This supports previous research as well as for ensuring the crabs’ care and maintenance during which has found that although P. bernhardus modulates its their brief experience of captivity. Harvey Broadhurst would behaviour to show measureable behavioural plasticity, this effect also like to thank Adam Bakewell for his invaluable advice is exceeded by the degree of behavioural consistency observed in and tutorials on how to use statistical computing programme R. this species (Briffa, Rundle and Fryer, 2008). The results pre- sented here suggest that investment in mechanisms required for behavioural plasticity and accurate modulation of responses is Author biography relatively low, with behavioural consistency and approximate modulation of responses favoured instead. Both the costs asso- Harvey graduated from the University of Hull in 2016 with a ciated with the production and maintenance of sensory and infor- BSc (Hons) in Zoology. Specializing in evolutionary biology mation processing systems, and variation in the level of and behavioural ecology, his most accomplished work ranged environmental heterogeneity, have been suggested as factors that from a field project on the symbiotic mutualisms of clownfish could explain the balance between plasticity and consistency and sea anemones, to a presentation on the evolution of the (Briffa, Rundle and Fryer, 2008). Previous research has remarked foot in early hominids. Harvey is currently working within on the limited extent of behavioural plasticity in hermit crabs the technology communications industry, conducting media (Hazlett, 1995). As consistent individual differences in behaviour relations for startups and high-growth tech companies. —as well as patterns of appropriate adjustment in boldness Eventually, he would like to develop a career in science com- across situations—have previously been used to suggest the pres- munication, promoting novel research in the field of zoology. ence of animal personalities (Brown, Jones and Braithwaite, 2005; Mowles, Cotton and Briffa, 2012; Rudin and Briffa, 2012), this limited behavioural plasticity may be due to the pres- ence of personality in hermit crabs, previously reported by Briffa, Statement of responsibility Rundle and Fryer (2008). Designing the study—L.J.M. and H.E.B., conducting experi- Further work is needed to elucidate the function of ments—H.E.B., analyzing the data—H.E.B., writing the increased emergence times in larger groups, and the mechan- manuscript—H.E.B. with feedback and input from L.J.M., isms by which individual crabs determine their emergence technical support—see acknowledgements, conceptual advice time across group sizes. We suggest that both immediate —L.J.M. threat of competition for shells and the detection of cues from previous fights may influence this decision. Clustering may still be associated with reduced predation risk, as grouping References carries anti-predator benefits across species (Krause and Ruxton, 2002) although larger groups may be more likely to Agrillo, C., Dadda, M., Serena, G. et al. (2008) Do fish count? attract predators, particularly if predators use movement to Spontaneous discrimination of quantity in female mosquitofish, detect their prey. Future studies examining the potential anti- Animal Cognition, 11, 495–503. predator benefits of clustering in P. bernhardus may therefore Agrillo, C., Dadda, M., Serena, G. et al. (2009) Use of number by fish, benefit from exploring locale-dependent variation in boldness PLoS One, 4, e4786. between sites with measurable differences in predation risk. Extended emergence times in hermit crabs have previously Benoit, M. D., Peeke, H. V. and Chang, E. S. (1997) Use of chemical cues been observed with the presence of predatory cues (Scarratt for shell preference by the hermit crab, Pagurus samuelis, Marine & and Godin, 1992), and therefore the role of predation risk in Freshwater Behaviour & Phy, 30, 45–54. determining emergence behaviour across group sizes would Briffa, M. (2013) Plastic proteans: reduced predictability in the face of shed light on whether this factor too plays a role in determin- predation risk in hermit crabs, Biology Letters, 9, 20130592. ing emergence times. Finally, how hermit crabs determine the size of the cluster and relative risk is another route for further Briffa, M. and Austin, M. (2009) Effects of predation threat on the struc- research. ture and benefits from vacancy chains in the hermit crab Pagurus bernhardus, Ethology : Formerly Zeitschrift fur Tierpsychologie, 115, 1029–1035. Supplementary Data Briffa, M., Bridger, D. and Biro, P. A. (2013) How does temperature affect Supplementary data are available at BIOHOR online. behaviour? Multilevel analysis of plasticity, personality and predict- ability in hermit crabs, Animal Behaviour, 86, 47–54. Briffa, M., Elwood, R. W. and Dick, J. T. A. (1998) Analysis of repeated sig- Acknowledgements nals during shell fights in the hermit crab Pagurus bernhardus, Proceedings of the Royal Society of London B: Biological Sciences, 265, We would like to thank aquatic technicians Rose Wilcox and 1467–1474. 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Group size and individual ‘personality’ influence emergence times in hermit crabs

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Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 BioscienceHorizons Volume 00 2018 10.1093/biohorizons/hzy011 ............................................................................................ ..................................................................... Research article Group size and individual ‘personality’ influence emergence times in hermit crabs Harvey Eliot Broadhurst and Lesley J. Morrell School of Environmental Sciences, University of Hull, Yorkshire, HU6 7RX, UK *Corresponding author: Harvey Eliot Broadhurst, Email: harv.broadhurst@gmail.com Supervisor: Lesley J. Morrell, School of Environmental Sciences (Biology), Hardy Building, University of Hull, Kingston-upon-Hull HU6 7RX. ............................................................................................ ..................................................................... Many animals benefit from aggregating due to the anti-predator effects associated with living in groups. Hermit crabs are known to form groups, or ‘clusters’, which may occur at sites of high shell availability. Clustering may also have anti-predator benefits, if individuals in larger clusters able to spend less time engaging in defensive behaviours such as hiding in their shells. Here, we test the hypothesis that crabs in larger clusters will emerge faster from their shells after an elicited startle response in the European hermit crab (Pagurus bernhardus). We found that individuals were generally consistent in their emergence times across group sizes (displaying ‘personality’ in relation to emergence time), but that group size influenced emergence time in P. bernhardus. In contrast to the hypothesis, crabs in larger clusters had longer emergence times relative to their own emergence times in smaller clusters. Suggested explanations for this effect include intra-specific competition for the gastropod shells that hermit crabs inhabit, as well as the possible release of chemical cues by crabs in larger clusters. Key words: hermit crabs, emergence time, personality, group size, behavioural consistency, Pagurus bernhardus Submitted on 3 March 2017; editorial decision on 29 October 2018 ............................................................................................ ..................................................................... in other activities (Pulliam, 1973; Cresswell and Quinn, Introduction 2011), which can also allow for cooperative warning, escape and defence behaviour (Krause and Ruxton, 2002). However, Group-living has been observed across a broad range of ani- as group size increases, individuals may also be subjected to mal taxa (Krause and Ruxton, 2002), and group size in par- increased competition for resources, which could be a limiting ticular has a major influence on the outcome of predator–prey factor in group size regulation (Grand and Dill, 1999). interactions, allowing group-living animals to manage their vulnerability to predation risk (Cresswell and Quinn, 2011). ‘Clustering’ has been identified as a behavioural strategy in The major costs associated with group-living, such as higher several hermit crab (superfamily Paguroidea) species, (Taylor, rate of attack from predators due to increased conspicuous- 1981; Gherardi and Vannini, 1989). Hermit crabs aggregate at ness, may be offset by anti-predator mechanisms (Uetz et al., sites of gastropod mortality, possibly to engage in ‘vacancy 2002). These mechanisms include the dilution of individual chain’ behaviour; the sequential distribution of the acquired risk (Foster and Treherne, 1981), the confusion of predators, gastropod shells that hermit crabs inhabit (Lewis and Rotjan, reducing attack success (Miller, 1922; Krakauer, 1995), 2009). When a hermit crab vacates its shell in order to occupy encounter-dilution (Turner and Pitcher, 1986) and selfish amore suitableone, other crabs have beenobserved ‘lining up’ herd effects (Hamilton, 1971). Grouping individuals also in order to vacate their own shells in favour of a newly avail- benefit from collective vigilance, with those in larger groups able one (De Waal, 2005). In P. bernhardus, the structure of able to reduce time spent scanning and increase time engaging these vacancy chains differs in the presence and absence of ............................................................................................... .................................................................. © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. predation risk (Briffa and Austin, 2009), but it is not known This study investigates whether P. bernhardus exhibits reac- whether the size of a cluster affects predation risk. Hermit tion norm variation across individuals when exposed to differ- crabs in the genus Pagurus do exhibit alarm responses when ent degrees of clustering (i.e. different group sizes). By exposed to the chemical cue of a crushed conspecific(Rittschof analyzing the variation in startle responses exhibited by indi- et al.,1992), and therefore clustering may serve an anti- vidual hermit crabs across several classes of group size, this predator function, with individuals benefiting from dilution or study explores whether emergence time is influenced by cluster- detection effects. However, larger clusters may also carry ing in P. bernhardus. If cluster size in this species is influenced increased risk of competition for shells from conspecifics. by both the anti-predator benefits and competition-associated costs of group-living, we expect to find a significant effect of Hermit crabs employ two major defences when exposed to group size on emergence time. If this species forms clusters as a potential predation: fleeing and refuging within their acquired response to predation risk, or gains anti-predator benefits from gastropod shells (Scarratt and Godin, 1992). If, on detecting a clustering, individuals are predicted to register shorter emer- predator, a crab decides to hide within the shell, then there is gence times in larger groups (where individual risk is lower) an associated second decision that determines the length of relative to their emergence times in smaller groups (where indi- time wherein the crab will remain hidden before emerging vidual risk is higher). Alternatively, if clustering carries once again (Briffa and Twyman, 2011). This decision to increased risk of competition, we might expect individuals in emerge is sensitive to the perceived risk of predation (Scarratt larger groups to remain in their shells for longer periods, to and Godin, 1992). For example, the presence of chemical reduce the risk of engaging in shell fights. Additionally, we pre- cues in the form of effluent from the predatory rock crab, dict that individual hermit crabs show significant patterns of Cancer productus, has been shown to significantly reduce individual consistency across different group sizes. emergence times in hermit crabs; whereas exposure to effluent from the herbivorous kelp crab, Pugettia productus, showed no difference from a saltwater control (Rosen, Schwarz and Methods Palmer, 2009). Withdrawal into a shell is also a response to competition: individuals are able to defend themselves from Data collection competitors in shell fights by retreating into their shells to avoid being forcibly removed (Courtene-Jones and Briffa, Sixty Pagurus bernhardus were collected from South Bay, 2014), and thus the decision to emerge may also be sensitive Scarborough, UK (54°16′12″N0°23′25″W) in October 2015. to the risk of competition. Emergence from a startle is also They were transported back to the laboratory at the consistent across individuals, with some showing consistently University of Hull within 4 h of collection, where they were longer recovery times, while others show consistently shorter kept in a holding tank (1.5-m circular diameter) that con- times (Briffa, Rundle and Fryer, 2008; Briffa and Twyman, tained steadily filtered aerated saltwater at a constant tem- 2011; Briffa, Bridger and Biro, 2013; Briffa, 2013). perature of 11°C. Crabs were given access to a large number of vacant shells of varying size (primarily common periwin- Rather than responding optimally across every situation kle, Littorina littorea; dog whelk, Nucella lapillus; and flat (behavioural plasticity), some individuals are constrained by top shell, Gibbula umbilicalis) and left to acclimatize to their consistent differences in behaviour over time or across con- new surroundings (and occupy a new shell if required) for texts (sometimes known as ‘animal personality’; Mathot and 72 h. Following acclimatization, 25 crabs were randomly Dingemanse, 2014). Startle responses may therefore be con- selected, weighed within their shells and individually num- sistent between individuals, forming a component of a ‘behav- bered on the shell using nail varnish, then placed inside plastic ioural syndrome’; which occurs when behaviours are containers (18 × 10 cm; one side meshed for aeration) within correlated across multiple behavioural categories (Jandt et al. the holding tank to isolate them and prevent shell-swapping 2014). One behaviour which is often reported as consistent is (Gherardi, 2006), a behaviour observed in the holding tank the ‘shyness-boldness’ axis, allowing for the classification of among unmarked individuals. Crabs were fed twice a week individuals as somewhere between ‘shy’ or ‘bold’ (Wilson on chopped mussel purchased from a local supermarket. et al., 1994). A bold individual would emerge rapidly from a Crabs were not sexed as previous studies have found that startle stimulus, while a shy would not (Briffa, Rundle and individual differences in startle response are independent of Fryer, 2008), and in P. bernhardus is correlated with each sex (Briffa, Rundle and Fryer, 2008). individual’s willingness to engage in ‘risky’ behaviour (Gherardi, Aquiloni and Tricarico, 2012). Behaviour however Startle response times for each marked individual were is also plastic in response to environmental conditions, and measured in five different group sizes (1, 2, 5, 10 and 20 indi- individuals can adapt their behaviour to the environment viduals). A group consisted of the marked individual and an (Pigliucci, 2001). In P. bernhardus, this plasticity is exceeded appropriate number of unmarked specimens selected haphaz- by individual consistency in boldness in response to high- and ardly from the holding tank. A circular observation container low-predation risk scenarios (Briffa, Rundle and Fryer, (35 cm diameter) was filled to a depth of 10 cm with water 2008). These between-individual differences over an environ- taken from the holding tank. The focal crab and the correct mental gradient (context) are termed ‘behavioural reaction number of unmarked individuals were placed onto a plate norms’ (Briffa, Bridger and Biro, 2013). (22 cm diameter), ensuring that the focal crab was positioned ............................................................................................... .................................................................. 2 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. in an inverted position to ensure it withdrew fully into its shell comparisons with all reference levels can be found in before observations began. All crabs were then gently tipped Appendix I). Body size was included as an additional fixed into the observation container. This method of eliciting a star- effect, and the identity of the crab was included as a random tle response is both successful and non-harmful in determin- effect to account for multiple measures on each individual ing response times of P. bernhardus (Briffa, Rundle and both within and between group sizes. Data were log- Fryer, 2008; Briffa, 2013). transformed to meet the assumptions of normality for statis- tical analysis, and non-significant interactions between body Latency to emerge from the shell was timed to the nearest size and group size were removed. second using a digital stopwatch from the point that the crab enters the observation container until the point at which its To investigate whether different individuals had predict- pereopods made contact with the base of the container ably different emergence times, an ANCOVA model was used (Briffa, 2013), when it is considered to be fully emerged. After on data from across all group sizes. This included the emer- emergence, the focal crab was returned to its individual con- gence time of the crab as the independent variable, the crab’s tainer, and the remaining crabs to the holding tank. The water identity as a dependent variable, and the group size that the in the observation container was changed between each trial. emergence time was obtained from as a covariate. A series of Each crab was given a maximum of 3 min to emerge before regression analyses were then used to further assess whether the trial was terminated (failure to emerge was recorded in an individual’s emergence time in one group size was a signifi- 61/375 trials). Startle responses were induced in each crab cant predictor of their respective emergence time in another twice a week for seven and a half weeks with each crab pro- group size. A total of 10 linear regressions were used in this viding up to 15 latencies in total, with 3 at each of the 5 group manner, with the mean emergence time of each crab in a given sizes to evaluate consistency of emergence time within a con- group size being regressed against their mean emergence time text (group size). Crabs were assigned a group size at random in another group size, until each group size had been com- during each data collection session, while ensuring that each pared against every other condition. To quantify individual experienced each group size a maximum of three times. consistency, repeatability was calculated using the intraclass correlation coefficient (r ); a measure of test–retest reliability IC Ethical approval was obtained from the School and (Uher, 2011). This was achieved using the R package ‘ICC’ Faculty Ethics Committees before the study began. At the end (Wolak, Fairbairn and Paulsen, 2012). of the experiment, the crabs were returned to the shore where they were collected from. Results Statistical analyses Does group size affect emergence time? To assess the relationship between group size and the time Accounting for individual variation in startle response, emer- that it took individuals to emerge from their shells, linear gence time increased with group size (Table 1, Fig. 1). There mixed-effects models were implemented using the package was no significant effect of body size on emergence time ‘nlme’ (Pinheiro et al., 2015) in R version 3.2.3 (R Core (Table 1). Treatment groups were compared against a group Team, 2015). Since the nature of the data involved several size of 2 as this was the group with the lowest mean emer- group size classes (1, 2, 5, 10 and 20), group size was treated gence time (Fig. 2). Crabs emerged faster in groups of 10 and as a categorical variable during analysis. Group sizes were 20 than they did in groups of 2 (Table 1). All other pairwise compared to a reference level of group size 2, as this was the comparisons can be found in Appendix I. group size with the lowest mean emergence time (pairwise Table 1. Linear mixed-effects models assessing the relationship between group size, body size and emergence time with individual identity as a random effect. Significant P-values are highlighted in bold. Value SE df tP Group size as a categorical variable (intercept: group size = 2) (intercept) 2.150 0.493 285 Group size = 1 0.225 0.161 285 1.391 0.165 Group size = 5 0.231 0.158 285 1.456 0.147 Group size = 10 0.400 0.160 285 2.492 0.013 Group size = 20 0.426 0.164 285 2.595 0.010 Body size 0.156 0.120 23 1.309 0.234 ............................................................................................... .................................................................. 3 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. consistently emerging rapidly from their shells, while those with longer emergence time (‘shy’ individuals) having consist- ently longer emergence times. The positive relationship between larger group size and longer emergence times suggest that competition with conspecifics, rather than the anti- predator benefits of grouping, are the key determinant of emergence decisions. Two related factors may explain this relationship: direct competition for gastropod shells and exposure to ‘fighting cues’ from conspecifics. Competition for gastropod shells is well-documented in hermit crabs (Elwood and Glass, 1981; Briffa, Elwood and Dick, 1998; Caven, Clayton and Sweet, 2012). Increased emergence times in larger groups may be explained by unin- tentional interference between individuals as they begin to move and emerge, such as shell-to-shell hitting or knocking. This type of disturbance would cause an emerging crab to retreat into their shell (Edmonds and Briffa, 2016), regardless of group size, but is probabilistically more likely as group size, and therefore density, increased. A tap to the shell during emergence could indicate to the crab that the risk of competi- tion was high, as it may be able to perceive whether the source of the tap was initiating a fight or not, and, given that crabs Figure 1. Bar graph showing mean responses of all crabs across group were likely to be in preferred-size shells, would have with- sizes with standard error represented as error bars. Significant effects drawn into the shell in defence (Elwood and Glass, 1981). of group size on emergence time are shown between a group size of 2 and 10, and 2 and 20. Any anti-predator benefits potentially gained from cluster- ing may have been offset by the risk of forced shell-eviction Do hermit crabs exhibit personality? from a conspecific. Indeed, in the wild, many members of the genus Pagurus are known to maintain a ‘rather large individ- Emergence times differed between crabs, even when account- ual distance’ instead of aggregating (Hazlett, 1968). Shell ing for variation caused by the different group sizes (group fights are often initiated by larger crabs and crabs that occupy size effect, F = 4.28, df = 1288, P = 0.03; individual effect, poor quality and/or unsuitably small shells (Dowds and F = 5.67, df = 24 288, P < 0.001; Fig. 3). In 8 out of 10 group Elwood, 1985), although we found no effect of size on emer- size comparisons, the emergence time registered by a crab in gence time. As crabs in this study were able to select from one group was found to be a significant predictor of how that unoccupied shells before experiments began, they may have crab would respond in other group sizes (Fig. 2; Table 2); this had low motivation to initiate a fight and maximal motivation shows consistency in the behaviour of crabs between treat- to retain their shells. As potential competition increases ments. No significant correlation was observed between emer- (increasing numbers of nearby conspecifics) motivation to gence times in group sizes of 1 and 10 (t = 1.67, P = 0.11), remain in the shell, defending it against competitions, may and 5 and 20 (t = 1.86, P = 0.08). have increased, as ‘shy’ behaviour is associated with higher Across all groups, emergence time was found to be gener- chances of successful shell-defence during a fight (Courtene- ally repeatable when measured with the intraclass correlation Jones and Briffa, 2014). As motivation to fight in hermit crabs coefficient (r = 0.26; Fig. 4). However, considering each is dependent on the quality of their shells (Elwood and Briffa, IC group size alone, significant repeatability was only found in a 2001), future studies may therefore benefit from examining group size of 2 (r = 0.56) and a group size of 20 (r = how individual emergence behaviour varies when crabs are IC IC 0.51). All other treatment groups returned an r value which housed in shells of varying size, quality and fit. IC had a 95% confidence interval inclusive of zero (Fig. 4), indic- Hermit crabs are also able to use chemical cues in order to ating non-significant repeatability despite the overall result. detect conspecifics and discriminate shells (Benoit, Peeke and Chang, 1997), and to distinguish between crabs that have recently fought and crabs that have not (Briffa and Williams, Discussion 2006). Exposure to these ‘fighting cues’ lengthens the amount of time a hermit crab spends withdrawn into its shell (Briffa The results suggest that both individual consistency and and Williams, 2006). Therefore, if the unmarked crabs had group size affect emergence time in hermit crabs. Individual been engaged in fights, the presence of fighting cues in the crabs were consistent in their behaviour across group sizes: water may have increased time spent withdrawn in the shell those with shorter emergence times (‘bolder’ individuals) ............................................................................................... .................................................................. 4 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. Figure 2. Significant positive correlations between crab emergence times in two group sizes; one larger than the other. Significance in these regressions represents predictability of an individual’s behaviour across treatments. Each data point represents an individual crab’s mean log emergence time at the specified group size. Group sizes are indicated on the axes of the graphs. in larger groups, where the probability of any one crab having The degree in which hermit crabs are able to detect discrete recently engaged in a fight would be increased, particularly as differences in conspecific group size is not known, forming a crowding is associated with increased aggression (Hazlett, potentially enlightening area for future investigation. The sug- 1968). In the green swordtail (Xiphophorus helleri), ‘eaves- gestion that animals are able to discriminate quantity through dropping’ on fights reduces a bystander’s propensity to the mental representation of numbers (counting)—as opposed engage in aggressive behaviour with the winning combatant to through non-numerical perceptible variables which differ post-fight (Earley and Dugatkin, 2002). with numerosity—has traditionally been restricted to mammalian ............................................................................................... .................................................................. 5 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 YYYY Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. Figure 3. Box and whisker diagrams for each crab showing variation in emergence time across all treatments. Grey box represents interquartile range with black line representing the median emergence time; outliers are represented as grey circles. Table 2. Pairwise comparisons of emergence time in five different group sizes. Significance (indicated by bold) represents predictability of an individual’s behaviour across treatments. Group size comparison tP n R 1 and 2 2.16 0.04 24 0.18 1 and 5 2.66 0.01 25 0.26 1 and 10 1.67 0.11 25 0.11 1 and 20 2.31 0.03 25 0.19 2 and 5 2.75 0.01 24 0.26 2 and 10 3.36 <0.01 24 0.34 2 and 20 3.05 <0.01 24 0.30 5 and 10 2.27 0.03 25 0.18 5 and 20 1.86 0.08 25 0.13 10 and 20 2.71 0.01 25 0.24 Figure 4. Intraclass correlation coefficients for all treatments and each group size separately, represented by data points and lines indicating the 95% confidence intervals. Grey dashed line represents zero. r IC models (Agrillo et al., 2009). However, previous studies have values with intervals not crossing zero are considered significant (black documented counting of conspecifics in mosquitofish data points and lines) whereas intervals crossing zero are considered (Gambusia holbrooki; Agrillo et al., 2008), as well as the non-significant (grey data points and lines). counting of landmarks in honey bees (Apis mellifera; Chittka and Geiger, 1995). The relationship between group size and emergence time discovered in this study therefore presents a In line with previous work (Briffa, Rundle and Fryer, 2008; novel opportunity to explore quantity discrimination in a Briffa and Twyman, 2011; Briffa, Bridger and Biro, 2013; Briffa, crustacean model. 2013), hermit crabs showed significant individual consistency in ............................................................................................... .................................................................. 6 Downloaded from https://academic.oup.com/biohorizons/article/doi/10.1093/biohorizons/hzy011/5253902 by DeepDyve user on 16 October 2022 Bioscience Horizons � Volume 00 2018 ............................................................................................... .................................................................. behaviour across group sizes, yet adjusted that behaviour in transportation of the hermit crabs that this project required, response to their environment. This supports previous research as well as for ensuring the crabs’ care and maintenance during which has found that although P. bernhardus modulates its their brief experience of captivity. Harvey Broadhurst would behaviour to show measureable behavioural plasticity, this effect also like to thank Adam Bakewell for his invaluable advice is exceeded by the degree of behavioural consistency observed in and tutorials on how to use statistical computing programme R. this species (Briffa, Rundle and Fryer, 2008). The results pre- sented here suggest that investment in mechanisms required for behavioural plasticity and accurate modulation of responses is Author biography relatively low, with behavioural consistency and approximate modulation of responses favoured instead. Both the costs asso- Harvey graduated from the University of Hull in 2016 with a ciated with the production and maintenance of sensory and infor- BSc (Hons) in Zoology. Specializing in evolutionary biology mation processing systems, and variation in the level of and behavioural ecology, his most accomplished work ranged environmental heterogeneity, have been suggested as factors that from a field project on the symbiotic mutualisms of clownfish could explain the balance between plasticity and consistency and sea anemones, to a presentation on the evolution of the (Briffa, Rundle and Fryer, 2008). Previous research has remarked foot in early hominids. Harvey is currently working within on the limited extent of behavioural plasticity in hermit crabs the technology communications industry, conducting media (Hazlett, 1995). As consistent individual differences in behaviour relations for startups and high-growth tech companies. —as well as patterns of appropriate adjustment in boldness Eventually, he would like to develop a career in science com- across situations—have previously been used to suggest the pres- munication, promoting novel research in the field of zoology. ence of animal personalities (Brown, Jones and Braithwaite, 2005; Mowles, Cotton and Briffa, 2012; Rudin and Briffa, 2012), this limited behavioural plasticity may be due to the pres- ence of personality in hermit crabs, previously reported by Briffa, Statement of responsibility Rundle and Fryer (2008). Designing the study—L.J.M. and H.E.B., conducting experi- Further work is needed to elucidate the function of ments—H.E.B., analyzing the data—H.E.B., writing the increased emergence times in larger groups, and the mechan- manuscript—H.E.B. with feedback and input from L.J.M., isms by which individual crabs determine their emergence technical support—see acknowledgements, conceptual advice time across group sizes. We suggest that both immediate —L.J.M. threat of competition for shells and the detection of cues from previous fights may influence this decision. Clustering may still be associated with reduced predation risk, as grouping References carries anti-predator benefits across species (Krause and Ruxton, 2002) although larger groups may be more likely to Agrillo, C., Dadda, M., Serena, G. et al. (2008) Do fish count? attract predators, particularly if predators use movement to Spontaneous discrimination of quantity in female mosquitofish, detect their prey. Future studies examining the potential anti- Animal Cognition, 11, 495–503. predator benefits of clustering in P. bernhardus may therefore Agrillo, C., Dadda, M., Serena, G. et al. (2009) Use of number by fish, benefit from exploring locale-dependent variation in boldness PLoS One, 4, e4786. between sites with measurable differences in predation risk. Extended emergence times in hermit crabs have previously Benoit, M. D., Peeke, H. V. and Chang, E. S. (1997) Use of chemical cues been observed with the presence of predatory cues (Scarratt for shell preference by the hermit crab, Pagurus samuelis, Marine & and Godin, 1992), and therefore the role of predation risk in Freshwater Behaviour & Phy, 30, 45–54. determining emergence behaviour across group sizes would Briffa, M. (2013) Plastic proteans: reduced predictability in the face of shed light on whether this factor too plays a role in determin- predation risk in hermit crabs, Biology Letters, 9, 20130592. ing emergence times. 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BioScience HorizonsOxford University Press

Published: Jan 1, 2018

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