Correlating context-specific boldness and physiological condition of female sand fiddler crabs (Uca pugilator) Rachel A. Decker & Blaine D. Griffen
Journal of Ethology ISSN 0289-0771 J Ethol DOI 10.1007/s10164-012-0338-9
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Author's personal copy J Ethol DOI 10.1007/s10164-012-0338-9
ARTICLE
Correlating context-specific boldness and physiological condition of female sand fiddler crabs (Uca pugilator) Rachel A. Decker • Blaine D. Griffen
Received: 22 March 2012 / Accepted: 14 June 2012 Ó Japan Ethological Society and Springer 2012
Abstract Consistent individual behavioral differences across ecological contexts are a recognized feature of animal populations. These differences can be expressed in two ways: context-specifically or context-generally. The former is characterized by consistent responses in one context (i.e. repeatability), whereas the latter by consistency that spans contexts (i.e. behavioral syndromes). The proximate causes of behavioral consistency remain unclear, yet there is evidence that physiology may couple the expression of some behavioral traits in unrelated contexts. We therefore explored the correlation between bold behavior of female sand fiddler crabs (Uca pugilator) and the condition of the hepatopancreas, an organ vital to crustacean metabolism and reproduction. We did this by taking replicate measurements of two risk-taking behaviors per individual in the contexts of predator avoidance and environment exploration, and examining correlations within and between these observations. We then determined the relationship of behavior with hepatopancreas mass and lipid content. Individual crabs responded consistently within each context. However, across-context correlations were absent, indicating that boldness is isolated, at least in the selected scenarios. Additionally, antiR. A. Decker B. D. Griffen Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA R. A. Decker (&) Marine Science Program, Department of Biological Sciences, Florida International University, 3000 NE 151st St, North Miami, FL 33181, USA e-mail:
[email protected] B. D. Griffen Marine Science Program, University of South Carolina, Columbia, SC 29208, USA
predator and exploratory behaviors were significantly influenced by size but not linked to hepatopancreas physiology. Our results show that context-specific trait expression may occur in the absence of a physiological correlate. Keywords Exploration Hepatopancreas Hepatosomatic index Hiding time Lipid
Introduction Consistent differences among individuals in response to identical stimuli is a recognized feature of natural populations (Boyer et al. 2010). Many studies suggest that both wild and domestic individuals exhibit behavior that is stable over time and/or across ecological contexts (Sih et al. 2004a, b; Wolf et al. 2007; Wilson and Godin 2009). In essence, an individual does not exhibit the same range of responses for a particular personality trait as is seen in the population as a whole (e.g., aggression, general activity level, sociability), but instead consistently expresses a limited subset of that range (Dingemanse et al. 2009). Therefore, many behavioral phenotypes exist for any given trait (Coleman and Wilson 1998), forming a continuum along which individuals can be organized by average intensity of expression (Dingemanse et al. 2009). Individuals at the poles of such a continuum exhibit opposite strategies for that trait, whereas intermediate strategists constitute the center. One of the most widely reported animal personality traits is boldness, defined as the tendency to take risks (Wilson et al. 2010). This trait has been documented empirically in more than 60 species across multiple taxa (Wolf et al. 2007). Evidence that bold behavior may be ecologically influential is growing. Positive correlations
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between boldness and numerous additional behaviors have been reported including: social dominance (Mettler and Shivik 2006), propensity to disperse (Rehage and Sih 2004), predation risk (de Azevedo and Young 2006), foraging success (Webster et al. 2007), and reproductive success (Dingemanse and Re´ale 2005; Reaney and Backwell 2007). These relationships indicate that boldness has the potential to influence individual functioning and success in a variety of scenarios. Personality traits such as boldness can be expressed in one of two ways (Sih et al. 2004b). The first of these is context-specific, in which expression is consistent in a single functional behavioral category (Sih et al. 2004a), such as feeding, mating, or predator avoidance. This type of expression is frequently referred to as repeatability. An example was reported in the dumpling squid (Euprymna tasmanica; Sinn and Moltschaniwskyj 2005). Consistent individual differences in boldness were found in both threat and feeding scenarios in individuals of this species; however, differences in boldness were not correlated across these two contexts. Individual squid were not generally bold or shy, but were flexible in their boldness depending on whether they were examining food or reacting to a threat (Sinn and Moltschaniwskyj 2005). The second type of expression is context-general, in which behavior is similar across multiple behavioral categories. This type of expression is referred to as a behavioral syndrome (Sih et al. 2004b). An example was documented in males of an Australian population of the fiddler crab Uca mjoebergi (Reaney and Backwell 2007). Consistent boldness in these individuals was found in three disparate ecological scenarios: hiding behavior following a predation threat, aggression with conspecifics, and surface activity levels. Additionally, boldness was positively correlated across these three contexts. Relative to their shy counterparts, bold males in this population repeatedly surfaced faster following a predation threat, were more likely to evict resident males from their burrows, and were active on the sediment surface for longer periods of time. Interestingly, they were also selected as mates more frequently by receptive females, suggesting a link between consistent behavior and reproductive success (Reaney and Backwell 2007). Context-specific and context-general expression have both been widely documented, yet the ecological and evolutionary reasons that a specific behavioral paradigm prevails in any given system remain unclear (Bergmu¨ller and Taborsky 2010). One possibility is that context-general expression arises if a trait is linked to physiology (Koolhaas et al. 1999; Re´ale et al. 2000; Garamszegi et al. 2012). Significant correlations between personality and physiology have been documented in numerous species (Wolf and Weissing 2010). For example, one study found
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that individual poeciliid fish exhibit strong behavioral correlations between shelter use, the tendency to leave shoalmates, and willingness to approach unfamiliar objects (Brachyraphis episcopi; Brown et al. 2005). Additionally, bold behavior in these individuals was negatively correlated with standard length, suggesting variation in metabolism (due to differences in body size) may be a mechanism shaping personality trait expression. Juveniles, which have higher size-specific metabolic needs than adults, may be predisposed to behave boldly to meet high energetic demands (Brown et al. 2005), suggesting that consistent behavior is at least partially determined by characteristics of internal physiology. As demonstrated in poeciliid fish, age and/or size may also have important impacts on personality traits. An animal’s interactions with its environment can change considerably over ontogeny (Brown et al. 2005). For example, in the fiddler crab Uca lactea perplexa, smaller individuals of both sexes were bolder and re-emerged from hiding more quickly than larger conspecifics following a predation threat (Jennions et al. 2003). In general, different demographic groups may exhibit natural variation in body size and function that influences their placement along the boldness continuum (Sih et al. 2004a). Here, we explore the consistency of individual variation in bold behavior of female Uca pugilator (sand fiddler crabs) within a South Carolina population. We examine whether boldness is context-general or context-specific, and whether there is a correlation between boldness and individual physiology. We do this in two ways. First, we quantify boldness in two widely used contexts in behavioral studies: predator avoidance and exploration of a novel environment (Wilson and Godin 2009). Boldness is exhibited in each of these contexts, respectively, by the tendency to emerge quickly from hiding and proactively investigating a new environment. Second, we examine correlations between observed behaviors and two aspects of physiology of the hepatopancreas, a digestive organ that stores nutrients and energy used in growth and reproduction in crustaceans (Gibson and Barker 1979; Plaistow et al. 2001). Specifically, we measured hepatopancreas mass and bulk lipid content, two indicators of physiological condition in crabs (mass: Yamaguchi 2001, 2003; lipids: Kyomo 1988; Kennish 1996; Quackenbush and Keeley 1988). We address a dichotomous hypothesis with this study that investigates the suggested link between physiology and behavioral expression (Brown et al. 2005; Biro et al. 2010; Wolf and Weissing 2010; Garamszegi et al. 2012). If boldness is context-general (individual crabs tend to act boldly or shyly in both contexts, demonstrating a behavioral syndrome), we predict that behavior will be correlated with the condition of the hepatopancreas. Conversely, we predict that if boldness is context-specific (crabs tend to act
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boldly in one context yet cautiously in the other, demonstrating repeatability but not a behavioral syndrome), there will be no relationship between behavior and the hepatopancreas. If either of these scenarios occurs, this would be consistent with a physiological basis for behavior. However, if either of the alternatives occur (context-general behavior and no physiological connection or context-specific behavior with a physiological connection), this would contradict the hypothesis that internal physiology drives context-general behavior.
Materials and methods Species and study site We conducted this study between May and August 2010 at North Inlet Estuary (33.3333°N, 79.1933°W) in Georgetown, South Carolina, USA. Within this estuary, fiddler crabs are the numerically dominant brachyuran inhabiting intertidal mud flats (Christy and Morgan 1998). These small, social deposit feeders excavate burrows in sandy or muddy sediment which they occupy at high tide (Crane 1975). They emerge from burrows at the onset of each low tide to forage in large, mixed-sex aggregations (Christy 1978). During these low-tide foraging periods hundreds to thousands will congregate in a single area, allowing for ease of observation and capture. Consequently, we conducted all field work during diurnal low tides. Behavioral test procedures We acquired two measurements of each behavior within this study to determine whether repeatability was present in the population. We limited our assays to two trials because more than two observations of each behavior do not significantly alter estimates of behavioral consistency (Bell et al. 2009). Behavioral tests were performed on all individuals within 48 h of our first interactions with that individual (described below) to ensure that physiological state did not alter substantially during observation and subsequently confound results. Energy stores in this species are capable of dramatic changes over short time periods. This has been demonstrated by the considerable effect of starvation on hepatopancreas condition, where lipid levels within the hepatopancreas, and subsequently hepatopancreas mass, decreased considerably over several days as a result of food deprivation (Speck and Urich 1969). Context 1: hiding in response to predation ‘‘Hiding time’’ was the initial behavioral trial for all sampled individuals and was recorded in the field.
Measurements were made by a single observer who chose a focal female, between 1 and 3 m away, in a foraging aggregation. Efforts were made over the course of the study to choose females of varying sizes. The observer approached the aggregation until the focal female retreated into a nearby burrow. A stop-watch was used to determine the amount of time between disappearance and emergence. Emergence was defined as the point at which the crab’s entire carapace was visible, as surfacing typically occurred slowly. Following emergence, the observer remained motionless until the focal crab resumed regular foraging activity or for 3 min, at which time approach and measurement were repeated. Female foraging occurred away from high intertidal areas where males were courting. Therefore, it is unlikely that females retreated into burrows where males were already present that may have aggressively ousted them Focal crabs were captured after two measurements were made and transported to a wet laboratory. Their dorsal carapace was labeled with a unique number written in permanent ink on a piece of colored electrical tape. All crabs were housed in a communal aquarium for 24–36 h before the second set of behavioral trials was begun. Crabs were starved during this time in order to standardize hunger state before further testing. Context 2: exploration of a novel environment We measured this behavior in the laboratory so as to (1) introduce crabs into a truly new and unfamiliar area, and (2) control the size and conditions within that area, ensuring each individual encountered the same conditions inside it. A rectangular glass aquarium (dimensions: 55 9 30 9 35 cm) served as the novel environment for trials within this context. In preparation, the aquarium sides were covered with opaque plastic to remove the influence of external visual cues. Additionally, the bottom of the aquarium was uniformly covered with approximately 2 cm of sediment that had been previously collected from the field and ashed in a muffle furnace at 550 °C for 5 h to remove organic content. After ashing, filtered seawater was added, as sediment with high water content is vital to natural fiddler crab functioning (Reinsel and Rittschof 1995). Removal of organic content was carried out in order to standardize ‘patch’ quality within the experimental arena. Behavior during trials was therefore not driven by response to heterogeneous organic content or interrupted by actual feeding. Finally, eight equally sized quadrants, each with an area of 206 cm2, were marked into the sediment as a means to assess exploratory movements of crabs during trials. Crabs were individually placed into the prepared aquarium under a plastic cup rigged to a pulley system.
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After a 10-min acclimation period, the cup was remotely raised and the crab given free range of the tank for an additional 10 min while a digital video camera recorded crab movements from directly above. From this video footage we quantified ‘‘searching space,’’ defined as the number of quadrants the crab entered with its entire body. Searching space observations included re-entering of quadrants, and therefore a crab could have a searching space value larger than the total number of quadrants in the aquarium if it was actively wandering throughout the trial. Trials were conducted twice with at least 2 h separating those for a single crab. Crabs were selected for the first trial at random until an entire group from the same hiding time sampling date had participated. That order was then repeated in the second round. Following completion of these trials, females were killed and their carapace width measured to the nearest 0.05 mm. They were stored in a -80 °C freezer until later dissection.
\2 % of ovigerous females were outside of this size range (Colby and Fonseca 1984). Because the hepatopancreas is closely tied to reproductive physiology, we chose to include only females of sizes known to be reproductively active. Statistical analysis Our sample consisted of 158 female crabs. Observations for each behavioral metric were not normally distributed and transformations did not substantially improve this. We therefore used nonparametric statistics. Analyses were conducted with the statistical programs SPSS v.17.0 and R v.2.11.1. We first explored the potentially confounding factor on hiding time of observer distance from the focal individual. This was recorded in meters for each trial and the results of a Kruskal–Wallis test indicated that observer distance at the time predation cues occurred did not affect hiding time duration (v2 = 10.347, n = 158, df = 5, P = 0.11).
Hepatopancreas and gonad analysis Size effects We quantified two metrics to assess individual crab physiological condition: the gonado-hepatosomatic index and bulk lipids. To conduct these analyses, crabs were thawed and the hepatopancreas and ovaries were removed through dorsal dissection. The cumulative dry weight of these organs was measured, as was the dry weight of the carapace and remaining organs. We then added these two weights together, yielding a total body weight. A gonadohepatosomatic index was calculated by expressing the weight of the hepatopancreas and ovaries as a ratio of the total body weight (Kyomo 1988). We next conducted bulk lipid extraction of the dried hepatopancreas and ovaries following the methods of Hara and Radin (1978). Following extraction, we weighed the isolated lipids and divided this value by the cumulative dry weight of the hepatopancreas and ovaries. The ovaries and hepatopancreas were combined in the above analyses because in most instances resolute separation of these organs was difficult. Only in some of the largest individuals, or those that happened to be in advanced reproductive phases, were the gonads easily differentiated from the surrounding hepatopancreas. Additionally, both organs contribute resources to egg yolk protein synthesis in female Uca pugilator (Quackenbush and Keeley 1988). For these reasons, we included both in determination of an individual’s physiological condition. Gonado-hepatosomatic index calculation and lipid extraction were carried out for a subset of 65 of the experimental crabs (just over 40 % of our sample). Only crabs between 10 and 18 mm carapace width were used, because a previous survey of Uca pugilator revealed that
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Our analysis revealed significant correlations between carapace width and each behavior (see ‘‘Results’’). We therefore investigated the effects of crab size on both hiding time and searching space using individual regression analyses, with each behavioral response from our four trials (two hiding time and two searching space trials) as response variables and crab carapace width as the predictor variable. We then repeated these same analyses using the average of the two trials of each type of behavior as response variables and crab carapace width as predictor variable. We subsequently removed the effect of crab size by using the residuals from these regressions in all analyses of personality trait expression and physiological correlations. Personality trait expression We used two-tailed Spearman rank correlation tests to examine the consistency of behavioral response within and between the two contexts. To determine if crabs behaved consistently across trials within each context, we calculated correlation coefficients between the residuals of the replicate behavioral trial regressions, described above. To determine if crabs behaved consistently across contexts, we calculated correlation coefficients between the residuals from the averaged trial regressions. A high frequency of relatively short hiding times was exhibited by our sample. Consequently, many of the observations were clustered in a small portion of the total range. To ensure that this feature of the hiding time data
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The lunar cycle, and corresponding tidal cycle, has a strong influence on fiddler crab sexual receptivity and energy reserves (Skov et al. 2005). Females within a population are usually split into two groups, each reproductively synched to one of two monthly spring tides. Therefore, sexual receptivity and engagement in mating behavior and copulation alternates between these groups after each 2-week semilunar cycle (Christy 1983). Hepatopancreas size and energy reserves are affected by the onset and duration of these cyclic mating behaviors as the bulk of energy used to carry them out is drawn from this organ. Given the known link between the 14-day tidal cycle, the 28-day lunar cycle, and the crab reproductive period, it was unclear whether we should expect a priori that crab physiology should follow a 14- or a 28-day cycle. We therefore conducted replicate nonlinear regressions using the equation for a sine wave where the wave frequency was set to 14 days and then to 28 days. Like all regressions, these tested for the strength of the relationship between two variables, in this case hepatopancreas condition and the cyclical effects of the tidal and lunar cycles. We used these regressions to remove the predictable influence of these natural phenomena on hepatopancreas physiology by fitting them to both the gonado-hepatosomatic index values and to the lipid values and calculated the resulting residuals. We then conducted Spearman rank correlation tests between the residuals from these sine wave regressions and the residuals of average behavioral responses (after removing the effects of crab size using linear regressions as described earlier).
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was not overly influential on our results, we performed a bootstrap analysis by randomly pairing the first hiding time observations with the second hiding time observations and then conducting a Spearman rank correlation test iterated 10,000 times. We then determined the proportion of these random pairings that yielded a stronger correlation than our observed correlation.
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Fig. 1 The relationship between Uca pugilator carapace width and individual average response for hiding time (a) and searching space (b). Least squares regression lines are shown for each relationship. Crabs appear to become increasingly cautious as they grow
The boldness continuum and personality trait expression Results Size effects Our analysis revealed weak but significant correlations between carapace width and each behavior. Relative to large crabs, smaller crabs tended to emerge sooner from hiding (linear regression: F1,156 = 24.99, P \ 0.001, R2 = 0.14; Fig. 1a) and to explore the novel environment more actively (linear regression: F1,156 = 32.269, P \ 0.001, R2 = 0.17; Fig. 1b).
A wide range of behavioral responses were exhibited for each behavior, revealing broad boldness continua in both contexts. Average hiding times ranged between 2.5 and 355 s (standard deviation = 84.044 s; Fig. 2a). Average searching space ranged from 0 to 81.5 quadrants (standard deviation = 209.120 quadrants; Fig. 2c). The boldness of individual crabs, corrected for size, was consistent within each context as indicated by a significant positive correlation between the residuals of replicate trials for both hiding time (Spearman rank: q = 0.604,
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(b) and searching space (d). Correlations between these observations were examined to determine if, correcting for the effect of size, crabs exhibited consistent risk-taking behavior within each context
P \ 0.001; Fig. 2b) and searching space (Spearman rank: q = 0.721, P \ 0.001; Fig. 2d). However, although crab behaviors were consistent within contexts, they were not consistent across contexts. Residuals of average hiding time and average searching space (again, corrected for size) were not significantly correlated (Spearman rank: q = -0.102, P = 0.204; Fig. 3). Additionally, none of the 10,000 random pairings of the first and second hiding time observations yielded a Spearman rank correlation rho with an absolute value larger than that found within this study. It is therefore highly
unlikely (P \ 0.0001) that the significant results associated with the predator avoidance context are the result of an abundance of clustered, short hiding times (Fig. 2b).
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Physiological correlates Neither the gonado-hepatosomatic index residuals nor the bulk lipid residuals (after accounting for the tidal cycle) showed a clear relationship with behavior, regardless of the selected sine wave frequency. The residuals of the 14-day frequency regression of lipid content and gonado-hepatosomatic index
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Discussion Size effects
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Carapace width influenced behavioral response in both the predator avoidance and exploration contexts. In both, smaller crabs tended to be bolder than large crabs (Fig. 1). Variation in size often results in differential predation risk, resulting in different predator avoidance strategies (Jennions et al. 2003). The presence of differences demonstrated here in risk-taking behavior based on body size is likely a result of variation in relative predation risk between large and small females within this population.
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were not significantly correlated with the residuals correcting for body size of average hiding time or average searching space (Table 1). The same held true for correlations between behavioral residuals and the 28-day frequency regression residuals (Table 2). Correlations were also determined between raw, non-regressed values. No significant relationships existed.
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Fig. 3 Residual average hiding time versus residual average searching space (after accounting for crab size). Correlations between these observations were examined to determine if crabs exhibited similar risk-taking behavior in both contexts
We observed unimodal frequency distributions in both hiding time and searching space (Fig. 2a, c). However, while we found a predominance of bold hiding time behavior in this population, we found the opposite for searching space, in which shy behavior predominated. The modal peak of this frequency distribution is prominent, comprised of 43 individuals that explored an average of two or fewer quadrants during the exploration trials (Fig. 2c). Over half of all sampled individuals are located in the range of zero to only ten quadrants entered (the maximum average of the two trials being 81.5). This evidence suggests a high frequency of shy responses in female Uca pugilator when confronted with a novel environment.
Table 1 Summary of correlations between residuals of Uca pugilator gonado-hepatosomatic index and lipid content 14-day frequency sine wave regressions, to account for the tidal cycle, and the residuals of behavioral metrics from regression on crab size Physiological regression residuals
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n = 65 in all cases Table 2 Summary of correlations between residuals of gonado-hepatosomatic index and lipid content 28-day frequency sine wave regressions, to account for the tidal cycle, and the residuals of behavioral metrics from regression on crab size Physiological regression residuals
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n = 65 in all cases
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Personality trait expression Context-specific behavioral expression appears to be the case in this population for the behaviors we examined. The behavior of individuals was consistent within specific contexts; however, clear and significant correlations across the two contexts were not present. Thus, crabs that emerged soon after a predation threat did not necessarily actively explore the novel environment. There are a number of other studies that have failed to find behavioral consistency across contexts (Coleman and Wilson 1998; Re´ale et al. 2000; Yang et al. 2001; Sinn and Moltschaniwskyj 2005). These studies suggest that context-specific trait expression may occur when differing selection regimes are acting on a single personality trait (Re´ale et al. 2000; Sinn and Moltschaniwskyj 2005). Bold behavior may present a similar dilemma, resulting in increased survival and fitness in one situation yet not in another (Coleman and Wilson 1998). Subsequently, context-specific boldness may be the case within the present study because distinct selective pressures are acting on predator avoidance and exploration behavior of Uca pugilator. These selective pressures may require differing responses effectively catered to each context, increasing survival and fitness (Re´ale et al. 2000). Expression of boldness in the contexts examined here may not have been evolutionarily coupled to allow for this. For example, hiding in burrows is the usual response to predation risk in this genus (Layne et al. 1997). However, this strategy also incurs costs, as foraging and mate searching cannot usually occur during time spent in refuge (Hugie 2004). Hiding therefore represents a trade-off, between access to resources and avoidance of predators. Individuals that minimize time spent hiding may incur an advantage, gaining longer periods of access to resources than more cautious individuals. Bold behavior may reward a crab that survives the potential predation risk associated with limited refuge use. In contrast, bold behavior in exploration may be detrimental for fiddler crabs. Predation risk increases for Uca tangeri that wander far from refuge of large conspecific aggregations (Ens et al. 1993). Additionally, white ibis (Eudocimus albus) are known to preferentially seek out and consume female Uca pugilator because they lack the large enlarged claw characteristic of males that effectively increases predator handling time (Bildstein et al. 1989). Females respond to increased relative vulnerability by ensuring that they are always able to quickly retreat into a nearby burrow when a predator appears (Christy 1983). Therefore, boldness in exploratory contexts that take individuals far from the safety of refuges of burrows and groups may not be favored in female fiddler crabs. Thus, the absence of context-general behavior in this species may
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reflect contrasting selective pressures for the two contexts examined. Physiological correlates Neither lipid content of the hepatopancreas nor the gonadohepatosomatic index, corrected for cyclic fluctuations imposed by the tide and sexual receptivity, explained variation in boldness. Although it has been demonstrated that the state of the hepatopancreas, especially lipid storage, is important to successful functioning within mature fiddler crabs (Quackenbush and Keeley 1988; Yamaguchi 2001), it appears hepatopancreas physiology does not couple individual bold behavior in predator avoidance and exploration contexts in this population. Such a physiological mechanism, underpinning general trait expression, may not allow the flexibility favored by natural selection for survival and increased fitness (Wilson and Godin 2009). The adaptive responses exhibited by female Uca pugilator, acting boldly in one context but not in another, would not be possible if an underlying mechanism were in place that constrained plasticity in boldness. The context-specific expression of boldness and the absence of a hepatopancreas-related physiological correlate support the claim that physiological constraints drive context-general behavior (Brown et al. 2005; Biro et al. 2010; Wolf and Weissing 2010).
Conclusion We have demonstrated the presence of context-specific boldness in females of the sand fiddler crab Uca pugilator. This context specificity is manifested in a predominance of bold phenotypes in hiding time behavior, but a predominance of caution in searching behavior. Our results do not support the presence of an underlying physiological basis for these behavioral patterns. It must be noted that it is possible that a different physiological metric, such as metabolic rate, is influencing personality within this population. The result that body size is related to boldness in both contexts suggests that a size-related correlate, such as metabolic rate, could be at work within the behavioral expression observed here. It is also possible that there is simply no biological link between boldness in hiding time and searching behavior and the physiology of energy storage and usage in sand fiddler crabs. The hepatopancreas may not be involved in the concerted organization of bold behaviors measured here. In addition to physiology, a number of other forces also influence personality trait expression including: evolutionary constraints, the nervous system (Zupanc 2010), environmental factors such as temperature (Biro et al.
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2010), and population factors such as social interactions (Bergmu¨ller and Taborsky 2010) and density (Korpela et al. 2011). Disentangling the relative contributions of these myriad forces, and identifying those responsible for the expression of specific traits, or for expression in specific contexts, remains an active area of research. Studies investigating proximate causes of personality trait expression should initially document correlations (or the absence thereof) across ecological contexts. The nature of these correlations, and their stability over time, may then point the way to the underlying mechanisms that control them. If a labile physiological mechanism is coupling certain behaviors then this correlation may be susceptible to change over time. Conversely, a mechanism that is genetically driven, or due to a more stable state, will not. Further studies on links between disparate contexts and their proximate causes will contribute to our knowledge of the origins and patterns of personality traits across phylogeny. Acknowledgments Our work was funded by the University of South Carolina. We thank M. Repetto for help with sample processing. Thanks also to S. Woodin, J. Dudycha, B. Toscano, and anonymous reviewers for helpful comments on earlier drafts. Finally, thanks to the Baruch Marine Research Reserve and its staff for the use of equipment and resources.
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