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

Abstract

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.

Full text

BioscienceHorizons
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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
Introduction
Group-living has been observed across a broad range of ani-
mal taxa (Krause and Ruxton, 2002), and group size in par-
ticular has a major influence on the outcome of predator–prey
interactions, allowing group-living animals to manage their
vulnerability to predation risk (Cresswell and Quinn, 2011).
The major costs associated with group-living, such as higher
rate of attack from predators due to increased conspicuous-
ness, may be offset by anti-predator mechanisms (Uetz et al.,
2002). These mechanisms include the dilution of individual
risk (Foster and Treherne, 1981), the confusion of predators,
reducing attack success (Miller, 1922;Krakauer, 1995),
encounter-dilution (Turner and Pitcher, 1986) and selfish
herd effects (Hamilton, 1971). Grouping individuals also
benefit from collective vigilance, with those in larger groups
able to reduce time spent scanning and increase time engaging
in other activities (Pulliam, 1973;Cresswell and Quinn,
2011), which can also allow for cooperative warning, escape
and defence behaviour (Krause and Ruxton, 2002). However,
as group size increases, individuals may also be subjected to
increased competition for resources, which could be a limiting
factor in group size regulation (Grand and Dill, 1999).
‘Clustering’has been identified as a behavioural strategy in
several hermit crab (superfamily Paguroidea) species, (Taylor,
1981;Gherardi and Vannini, 1989). Hermit crabs aggregate at
sites of gastropod mortality, possibly to engage in ‘vacancy
chain’behaviour; the sequential distribution of the acquired
gastropod shells that hermit crabs inhabit (Lewis and Rotjan,
2009). When a hermit crab vacates its shell in order to occupy
amoresuitableone,othercrabshavebeenobserved‘lining up’
in order to vacate their own shells in favour of a newly avail-
able one (De Waal, 2005). In P. bernhardus, the structure of
these vacancy chains differs in the presence and absence of
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predation risk (Briffa and Austin, 2009), but it is not known
whether the size of a cluster affects predation risk. Hermit
crabs in the genus Pagurus do exhibit alarm responses when
exposed to the chemical cue of a crushed conspecific(
Rittschof
et al.,1992
), and therefore clustering may serve an anti-
predator function, with individuals benefiting from dilution or
detection effects. However, larger clusters may also carry
increased risk of competition for shells from conspecifics.
Hermit crabs employ two major defences when exposed to
potential predation: fleeing and refuging within their acquired
gastropod shells (Scarratt and Godin, 1992). If, on detecting a
predator, a crab decides to hide within the shell, then there is
an associated second decision that determines the length of
time wherein the crab will remain hidden before emerging
once again (Briffa and Twyman, 2011). This decision to
emerge is sensitive to the perceived risk of predation (Scarratt
and Godin, 1992). For example, the presence of chemical
cues in the form of effluent from the predatory rock crab,
Cancer productus, has been shown to significantly reduce
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
Palmer, 2009). Withdrawal into a shell is also a response to
competition: individuals are able to defend themselves from
competitors in shell fights by retreating into their shells to
avoid being forcibly removed (Courtene-Jones and Briffa,
2014), and thus the decision to emerge may also be sensitive
to the risk of competition. Emergence from a startle is also
consistent across individuals, with some showing consistently
longer recovery times, while others show consistently shorter
times (Briffa, Rundle and Fryer, 2008;Briffa and Twyman,
2011;Briffa, Bridger and Biro, 2013;Briffa, 2013).
Rather than responding optimally across every situation
(behavioural plasticity), some individuals are constrained by
consistent differences in behaviour over time or across con-
texts (sometimes known as ‘animal personality’;Mathot and
Dingemanse, 2014). Startle responses may therefore be con-
sistent between individuals, forming a component of a ‘behav-
ioural syndrome’; which occurs when behaviours are
correlated across multiple behavioural categories (Jandt et al.
2014). One behaviour which is often reported as consistent is
the ‘shyness-boldness’axis, allowing for the classification of
individuals as somewhere between ‘shy’or ‘bold’(Wilson
et al., 1994). A bold individual would emerge rapidly from a
startle stimulus, while a shy would not (Briffa, Rundle and
Fryer, 2008), and in P. bernhardus is correlated with each
individual’s willingness to engage in ‘risky’behaviour
(Gherardi, Aquiloni and Tricarico, 2012). Behaviour however
is also plastic in response to environmental conditions, and
individuals can adapt their behaviour to the environment
(Pigliucci, 2001). In P. bernhardus, this plasticity is exceeded
by individual consistency in boldness in response to high- and
low-predation risk scenarios (Briffa, Rundle and Fryer,
2008). These between-individual differences over an environ-
mental gradient (context) are termed ‘behavioural reaction
norms’(Briffa, Bridger and Biro, 2013).
This study investigates whether P. bernhardus exhibits reac-
tion norm variation across individuals when exposed to differ-
ent degrees of clustering (i.e. different group sizes). By
analyzing the variation in startle responses exhibited by indi-
vidual hermit crabs across several classes of group size, this
study explores whether emergence time is influenced by cluster-
ing in P. bernhardus. If cluster size in this species is influenced
by both the anti-predator benefits and competition-associated
costs of group-living, we expect to find a significant effect of
group size on emergence time. If this species forms clusters as a
response to predation risk, or gains anti-predator benefits from
clustering, individuals are predicted to register shorter emer-
gence times in larger groups (where individual risk is lower)
relative to their emergence times in smaller groups (where indi-
vidual risk is higher). Alternatively, if clustering carries
increased risk of competition, we might expect individuals in
larger groups to remain in their shells for longer periods, to
reduce the risk of engaging in shell fights. Additionally, we pre-
dict that individual hermit crabs show significant patterns of
individual consistency across different group sizes.
Methods
Data collection
Sixty Pagurus bernhardus were collected from South Bay,
Scarborough, UK (54°16′12″N0°23′25″W) in October 2015.
They were transported back to the laboratory at the
University of Hull within 4 h of collection, where they were
kept in a holding tank (1.5-m circular diameter) that con-
tained steadily filtered aerated saltwater at a constant tem-
perature of 11°C. Crabs were given access to a large number
of vacant shells of varying size (primarily common periwin-
kle, Littorina littorea; dog whelk, Nucella lapillus; and flat
top shell, Gibbula umbilicalis) and left to acclimatize to their
new surroundings (and occupy a new shell if required) for
72 h. Following acclimatization, 25 crabs were randomly
selected, weighed within their shells and individually num-
bered on the shell using nail varnish, then placed inside plastic
containers (18 ×10 cm; one side meshed for aeration) within
the holding tank to isolate them and prevent shell-swapping
(Gherardi, 2006), a behaviour observed in the holding tank
among unmarked individuals. Crabs were fed twice a week
on chopped mussel purchased from a local supermarket.
Crabs were not sexed as previous studies have found that
individual differences in startle response are independent of
sex (Briffa, Rundle and Fryer, 2008).
Startle response times for each marked individual were
measured in five different group sizes (1, 2, 5, 10 and 20 indi-
viduals). A group consisted of the marked individual and an
appropriate number of unmarked specimens selected haphaz-
ardly from the holding tank. A circular observation container
(35 cm diameter) was filled to a depth of 10 cm with water
taken from the holding tank. The focal crab and the correct
number of unmarked individuals were placed onto a plate
(22 cm diameter), ensuring that the focal crab was positioned
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in an inverted position to ensure it withdrew fully into its shell
before observations began. All crabs were then gently tipped
into the observation container. This method of eliciting a star-
tle response is both successful and non-harmful in determin-
ing response times of P. bernhardus (Briffa, Rundle and
Fryer, 2008;Briffa, 2013).
Latency to emerge from the shell was timed to the nearest
second using a digital stopwatch from the point that the crab
enters the observation container until the point at which its
pereopods made contact with the base of the container
(Briffa, 2013), when it is considered to be fully emerged. After
emergence, the focal crab was returned to its individual con-
tainer, and the remaining crabs to the holding tank. The water
in the observation container was changed between each trial.
Each crab was given a maximum of 3 min to emerge before
the trial was terminated (failure to emerge was recorded in
61/375 trials). Startle responses were induced in each crab
twice a week for seven and a half weeks with each crab pro-
viding up to 15 latencies in total, with 3 at each of the 5 group
sizes to evaluate consistency of emergence time within a con-
text (group size). Crabs were assigned a group size at random
during each data collection session, while ensuring that each
experienced each group size a maximum of three times.
Ethical approval was obtained from the School and
Faculty Ethics Committees before the study began. At the end
of the experiment, the crabs were returned to the shore where
they were collected from.
Statistical analyses
To assess the relationship between group size and the time
that it took individuals to emerge from their shells, linear
mixed-effects models were implemented using the package
‘nlme’(Pinheiro et al., 2015) in R version 3.2.3 (R Core
Team, 2015). Since the nature of the data involved several
group size classes (1, 2, 5, 10 and 20), group size was treated
as a categorical variable during analysis. Group sizes were
compared to a reference level of group size 2, as this was the
group size with the lowest mean emergence time (pairwise
comparisons with all reference levels can be found in
Appendix I). Body size was included as an additional fixed
effect, and the identity of the crab was included as a random
effect to account for multiple measures on each individual
both within and between group sizes. Data were log-
transformed to meet the assumptions of normality for statis-
tical analysis, and non-significant interactions between body
size and group size were removed.
To investigate whether different individuals had predict-
ably different emergence times, an ANCOVA model was used
on data from across all group sizes. This included the emer-
gence time of the crab as the independent variable, the crab’s
identity as a dependent variable, and the group size that the
emergence time was obtained from as a covariate. A series of
regression analyses were then used to further assess whether
an individual’s emergence time in one group size was a signifi-
cant predictor of their respective emergence time in another
group size. A total of 10 linear regressions were used in this
manner, with the mean emergence time of each crab in a given
group size being regressed against their mean emergence time
in another group size, until each group size had been com-
pared against every other condition. To quantify individual
consistency, repeatability was calculated using the intraclass
correlation coefficient (r
IC
); a measure of test–retest reliability
(Uher, 2011). This was achieved using the R package ‘ICC’
(Wolak, Fairbairn and Paulsen, 2012).
Results
Does group size affect emergence time?
Accounting for individual variation in startle response, emer-
gence time increased with group size (Table 1, Fig. 1). There
was no significant effect of body size on emergence time
(Table 1). Treatment groups were compared against a group
size of 2 as this was the group with the lowest mean emer-
gence time (Fig. 2). Crabs emerged faster in groups of 10 and
20 than they did in groups of 2 (Table 1). All other pairwise
comparisons can be found in Appendix I.
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
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Do hermit crabs exhibit personality?
Emergence times differed between crabs, even when account-
ing for variation caused by the different group sizes (group
size effect, F=4.28, df =1288, P=0.03; individual effect,
F=5.67, df =24 288, P<0.001; Fig. 3). In 8 out of 10 group
size comparisons, the emergence time registered by a crab in
one group was found to be a significant predictor of how that
crab would respond in other group sizes (Fig. 2; Table 2); this
shows consistency in the behaviour of crabs between treat-
ments. No significant correlation was observed between emer-
gence times in group sizes of 1 and 10 (t=1.67, P=0.11),
and 5 and 20 (t=1.86, P=0.08).
Across all groups, emergence time was found to be gener-
ally repeatable when measured with the intraclass correlation
coefficient (r
IC
=0.26; Fig. 4). However, considering each
group size alone, significant repeatability was only found in a
group size of 2 (r
IC
=0.56) and a group size of 20 (r
IC
=
0.51). All other treatment groups returned an r
IC
value which
had a 95% confidence interval inclusive of zero (Fig. 4), indic-
ating non-significant repeatability despite the overall result.
Discussion
The results suggest that both individual consistency and
group size affect emergence time in hermit crabs. Individual
crabs were consistent in their behaviour across group sizes:
those with shorter emergence times (‘bolder’individuals)
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
were likely to be in preferred-size shells, would have with-
drawn into the shell in defence (Elwood and Glass, 1981).
Any anti-predator benefits potentially gained from cluster-
ing may have been offset by the risk of forced shell-eviction
from a conspecific. Indeed, in the wild, many members of the
genus Pagurus are known to maintain a ‘rather large individ-
ual distance’instead of aggregating (Hazlett, 1968). Shell
fights are often initiated by larger crabs and crabs that occupy
poor quality and/or unsuitably small shells (Dowds and
Elwood, 1985), although we found no effect of size on emer-
gence time. As crabs in this study were able to select from
unoccupied shells before experiments began, they may have
had low motivation to initiate a fight and maximal motivation
to retain their shells. As potential competition increases
(increasing numbers of nearby conspecifics) motivation to
remain in the shell, defending it against competitions, may
have increased, as ‘shy’behaviour is associated with higher
chances of successful shell-defence during a fight (Courtene-
Jones and Briffa, 2014). As motivation to fight in hermit crabs
is dependent on the quality of their shells (Elwood and Briffa,
2001), future studies may therefore benefit from examining
how individual emergence behaviour varies when crabs are
housed in shells of varying size, quality and fit.
Hermit crabs are also able to use chemical cues in order to
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,
2006). Exposure to these ‘fighting cues’lengthens the amount
of time a hermit crab spends withdrawn into its shell (Briffa
and Williams, 2006). Therefore, if the unmarked crabs had
been engaged in fights, the presence of fighting cues in the
water may have increased time spent withdrawn in the shell
Figure 1. Bar graph showing mean responses of all crabs across group
sizes with standard error represented as error bars. Significant effects
of group size on emergence time are shown between a group size of 2
and 10, and 2 and 20.
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in larger groups, where the probability of any one crab having
recently engaged in a fight would be increased, particularly as
crowding is associated with increased aggression (Hazlett,
1968). In the green swordtail (Xiphophorus helleri), ‘eaves-
dropping’on fights reduces a bystander’s propensity to
engage in aggressive behaviour with the winning combatant
post-fight (Earley and Dugatkin, 2002).
The degree in which hermit crabs are able to detect discrete
differences in conspecific group size is not known, forming a
potentially enlightening area for future investigation. The sug-
gestion that animals are able to discriminate quantity through
the mental representation of numbers (counting)—as opposed
to through non-numerical perceptible variables which differ
with numerosity—has traditionally been restricted to mammalian
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.
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models (Agrillo et al., 2009). However, previous studies have
documented counting of conspecifics in mosquitofish
(Gambusia holbrooki;Agrillo et al., 2008), as well as the
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
novel opportunity to explore quantity discrimination in a
crustacean model.
In line with previous work (Briffa, Rundle and Fryer, 2008;
Briffa and Twyman, 2011;Briffa, Bridger and Biro, 2013;Briffa,
2013), hermit crabs showed significant individual consistency in
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 nR
2
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
values with intervals not crossing zero are considered significant (black
data points and lines) whereas intervals crossing zero are considered
non-significant (grey data points and lines).
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behaviour across group sizes, yet adjusted that behaviour in
response to their environment. This supports previous research
which has found that although P. bernhardus modulates its
behaviour to show measureable behavioural plasticity, this effect
is exceeded by the degree of behavioural consistency observed in
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
relatively low, with behavioural consistency and approximate
modulation of responses favoured instead. Both the costs asso-
ciated with the production and maintenance of sensory and infor-
mation processing systems, and variation in the level of
environmental heterogeneity, have been suggested as factors that
could explain the balance between plasticity and consistency
(Briffa, Rundle and Fryer, 2008). Previous research has remarked
on the limited extent of behavioural plasticity in hermit crabs
(Hazlett, 1995). As consistent individual differences in behaviour
—as well as patterns of appropriate adjustment in boldness
across situations—have previously been used to suggest the pres-
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,
Rundle and Fryer (2008).
Further work is needed to elucidate the function of
increased emergence times in larger groups, and the mechan-
isms by which individual crabs determine their emergence
time across group sizes. We suggest that both immediate
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
carries anti-predator benefits across species (Krause and
Ruxton, 2002) although larger groups may be more likely to
attract predators, particularly if predators use movement to
detect their prey. Future studies examining the potential anti-
predator benefits of clustering in P. bernhardus may therefore
benefit from exploring locale-dependent variation in boldness
between sites with measurable differences in predation risk.
Extended emergence times in hermit crabs have previously
been observed with the presence of predatory cues (Scarratt
and Godin, 1992), and therefore the role of predation risk in
determining emergence behaviour across group sizes would
shed light on whether this factor too plays a role in determin-
ing emergence times. Finally, how hermit crabs determine the
size of the cluster and relative risk is another route for further
research.
Supplementary Data
Supplementary data are available at BIOHOR online.
Acknowledgements
We would like to thank aquatic technicians Rose Wilcox and
Alan Smith for their assistance in the collection and
transportation of the hermit crabs that this project required,
as well as for ensuring the crabs’care and maintenance during
their brief experience of captivity. Harvey Broadhurst would
also like to thank Adam Bakewell for his invaluable advice
and tutorials on how to use statistical computing programme R.
Author biography
Harvey graduated from the University of Hull in 2016 with a
BSc (Hons) in Zoology. Specializing in evolutionary biology
and behavioural ecology, his most accomplished work ranged
from a field project on the symbiotic mutualisms of clownfish
and sea anemones, to a presentation on the evolution of the
foot in early hominids. Harvey is currently working within
the technology communications industry, conducting media
relations for startups and high-growth tech companies.
Eventually, he would like to develop a career in science com-
munication, promoting novel research in the field of zoology.
Statement of responsibility
Designing the study—L.J.M. and H.E.B., conducting experi-
ments—H.E.B., analyzing the data—H.E.B., writing the
manuscript—H.E.B. with feedback and input from L.J.M.,
technical support—see acknowledgements, conceptual advice
—L.J.M.
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