Mark Briffa

Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus

Many phenotypic traits show plasticity but behaviour is often considered the ‘most plastic’ aspect of phenotype as it is likely to show the quickest response to temporal changes in conditions or ‘situation’. However, it has also been noted that constraints on sensory acuity, cognitive structure and physiological capacities place limits on behavioural plasticity. Such limits to plasticity may generate consistent differences in behaviour between individuals from the same population. It has recently been suggested that these consistent differences in individual behaviour may be adaptive and the term ‘animal personalities’ has been used to describe them. In many cases, however, a degree of both behavioural plasticity and relative consistency is probable. To understand the possible functions of animal personalities, it is necessary to determine the relative strength of each tendency and this may be achieved by comparison of statistical effect sizes for tests of difference and concordance. Here, we describe a new statistical framework for making such comparisons and investigate cross-situational plasticity and consistency in the duration of startle responses in the European hermit crab Pagurus bernhardus, in the field and the laboratory. The effect sizes of tests for behavioural consistency were greater than for tests of behavioural plasticity, indicating for the first time the presence of animal personalities in a crustacean model.

Unpredictable animals: individual differences in intraindividual variability (IIV)

When an individual is repeatedly observed or tested in the same context, it does not always express the same behaviour. Intraindividual variability (IIV) refers to the short-term, unpredictable, reversible variation in behaviour that often occurs in this situation. Although individual differences in IIV have been well documented in humans, this topic has been virtually ignored by researchers studying other animals. Here, we review evidence from humans and animals that IIV can vary in important ways across individuals (e.g. as a function of age or prior experience) and that individual differences in IIV may be related to differences in performance. However, most statistical models currently used to study individual differences in behaviour in animals rely on the assumption that IIV does not vary across individuals. Using ‘boldness’ data for hermit crabs, Pagurus bernhardus, and Ward’s damselfish, Pomacentrus wardi, we show how to measure IIV when behaviour systematically changes over a series of observations (e.g. as a result of habituation), and how to avoid the adverse effects of censored data on estimates of IIV. After controlling for systematic changes in behaviour over time, we observed strong, significant individual differences in IIV in both species. That is, some individuals were much more predictable in the same situation than were others. We conclude by discussing proximate and ultimate factors that might have contributed to interindividual variation in IIV in these species, and the implications of our findings for methods currently used to study individual differences in behaviour in animals.

Use of energy reserves in fighting hermit crabs

When animals engage in fights they face a series of decisions, which are based on the value of the contested resource and either their relative or their absolute fighting ability. Certain correlates of fighting ability or ‘resource holding potential’ such as body size are fixed but physiological correlates are expected to vary during the encounter. We examine the role of energy reserves in determining fight outcomes and parameters during ‘shell fighting’ in hermit crabs. During these fights, the two contestants perform very different roles of attacker and defender. We show that the balance of the total energy pool, in the form of glucose and glycogen, determines the ability of defenders to resist eviction from their shells. Low glucose in evicted defenders is not caused by depletion of energy reserves, rather mobilization of glycogen appears to be the result of a strategic decision about whether to resist effectively, based on the perceived fighting ability of the attacker. Attackers, however, always initiate the fight so such a decision for this role appears unlikely. In addition to influencing decisions and ability during fights, physiological correlates of fighting ability can in turn be influenced by strategic decisions.

Decision rules, energy metabolism and vigour of hermit–crab fights

Aggressive interactions between animals are often settled by the use of repeated signals that reduce the risk of injury from combat but are expected to be costly. The accumulation of lactic acid and the depletion of energy stores may constrain activity rates during and after fights and thus represent significant costs of signalling. We tested this by analysing the concentrations of lactate and glucose in the haemolymph of hermit crabs following agonistic interactions over the ownership of the gastropod shells that they inhabit. Attackers and defenders play distinct roles of sender and receiver that are fixed for the course of the encounter. Attackers perform bouts of ‘shell rapping’, which vary in vigour between attackers and during the course of the encounter, and are a key predictor of victory. In contrast to the agonistic behaviour of other species, we can quantify the vigour of fighting. We demonstrate, to our knowledge for the first time, an association between the vigour of aggressive activity and a proximate cost of signalling. We show that the lactate concentration in attackers increases with the amount of shell rapping, and that this appears to constrain the vigour of subsequent rapping. Furthermore, attackers, but not defenders, give up when the concentration of lactate is high. Glucose levels in attackers also increase with the amount of rapping they perform, but do not appear to influence their decision to give up. Defenders are more likely to lose when they have particularly low levels of glucose. We conclude that the two roles use different decision rules during these encounters.

Analysis of repeated signals during shell fights in the hermit crab Pagurus bernhardus.

Shell exchanges between hermit crabs may occur after a period of shell rapping, when the initiating or attacking crab brings its shell rapidly and repeatedly into contact with the shell of the non–initiator or defender, in a series of bouts. There are two opposing models of hermit crab shell exchange and the function of shell rapping. The negotiation model views shell exchange as a mutualistic activity, in which the initiator supplies information about the quality of its shell via the fundamental frequency of the rapping sound. The aggression model views shell rapping as either detrimental to the defending crab, or as providing it with information about the initiators ability or motivation to continue, or both. The negotiation model makes no predictions about the temporal pattern of rapping, but under the aggression model it would be expected that crabs that rapped more vigorously would be more likely to effect an exchange. Repeating the signal could be expected under either model. Crabs that achieve an exchange rap more vigorously, rapping is more persistent when a clear gain in shell quality may be achieved, and the vigour is greater when the relative resource–holding potential (or ‘fighting ability’) is high. These findings support the aggression model rather than the negotiation model. Contrary to the predictions of game theory, crabs that do not effect an exchange appear to signal that they are about to give up. The data suggest that rapping is performed repeatedly because the accumulation of all of the performances acts as a signal of stamina.

How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs

When animals are observed on multiple occasions, consistent between-individual differences in behaviour, often referred to as animal personality, may be observed. However, this does not mean that the behaviour of a given individual is readily predictable. While some individuals show low levels of variation around their behavioural mean, others show high levels of variation, and there may be significant between-individual differences in this intraindividual variation (‘IIV’) in behaviour. While it has been suggested that IIV might reduce susceptibility to predators, little is known about the functions or causation of IIV. We investigated the effects of temperature on the startle response duration of hermit crabs, Pagurus bernhardus. For poikilothermic animals, temperature has a direct and multiplicative influence on metabolic rate, which in turn is expected to influence behaviour because of its effect on energy requirements. At the level of mean startle response durations, the effect of temperature was dependent on treatment order; within treatment orders, individuals showed different reaction norms. In contrast, at the level of IIV, while the presence of significant between-individual differences was dependent on treatment order, there was a clear unidirectional effect in both treatment orders for individuals to be less predictable at higher temperature. Thus, predictability in behaviour appears to vary with a key environmental variable that is known to influence energy requirements and potentially the level of risk that individuals are willing to accept.

Power of shell-rapping signals influences physiological costs and subsequent decisions during hermit crab fights

Understanding the costs of signals used in fights is the key to understanding decisions made by contestants. Hermit crabs use shell rapping. This is a clearly defined agonistic signal, which can be quantified in temporal terms and in the power of the key shell-rapping signal component. We examine the relationship between the power expended by attacking hermit crabs and their consequent lactate levels. High power expenditure over the whole fight leads to high lactate, and attackers give up when lactate is high. Some defenders give up early in fights, particularly if the power of raps in early bouts they receive is high. These defenders and those not allowed to fight have low glucose, but those that successfully resist eviction have high glucose. Glucose is mobilized in an attempt to resist; nevertheless, some defenders that attempt resistance are still evicted by persistent attackers. Thus, early power of the signal is a major determinant of success for attackers, albeit at a cost. These data show the link between power, repetition of a signal, metabolic consequences and decisions of contestants in fights. The different activities, decisions and costs of the two roles are not adequately described by existing models of contests.

Reduced sea water pH disrupts resource assessment and decision making in the hermit crab Pagurus bernhardus

The decisions that animals make are based on information gathered from their environment, and can have consequences for their fitness and survival. Such processes can be disrupted by environmental change. Hermit crabs find and select the gastropod shells they inhabit using chemical and visual cues, and tactile assessment. The choice of an optimal shell is important since it provides shelter against environmental extremes and protection against predators; inhabiting a suboptimal shell can also reduce fecundity. Hermit crabs are subject to cyclical reductions in the pH of the water in the intertidal rock pools that they inhabit, and such reductions may be further exacerbated by climate change. Reduced sea water pH, a consequence of ocean acidification and leaks from geological storage sites, has already been shown to disrupt the behaviour of marine animals. We investigated the effects of reduced sea water pH on the shell assessment and selection behaviour of the hermit crab Pagurus bernhardus. Under highly reduced pH conditions (pH 6.8) crabs were less likely to change from a suboptimal to an optimal shell than those in untreated sea water; those that did change shells took longer to do so. Crabs in the reduced pH treatment also showed significantly lower antennular flicking rates (the ‘sniffing’ response in decapods) and reduced movement. Thus, a reduction in sea water pH disrupts the resource assessment and decision-making processes of these crabs, indicating that the ability to acquire a vital resource may be influenced by both naturally occurring environmental cycles and anthropogenically induced environmental change.

Rapid change in energy status in fighting animals: causes and effects of strategic decisions

Energetic costs of fighting, such as high lactate or low glucose, have been shown in a range of species to correlate with the decisions made by each opponent, particularly the decision by one opponent, the ‘loser’, to end the fight by ‘giving up’. Studies based on complete fights of differing duration, however, do not provide information on the changes in the physiological correlates of fighting that may take place during the course of the encounter, or how these changes may influence the capability and decisions of the contestants. We interrupted fights between hermit crabs, Pagurus bernhardus, at specific points, and related energy status to the preceding activities. Costs rose quickly with a rapid accumulation of lactic acid in attackers and declining muscular glycogen in defenders. Changes in physiological status appeared much earlier than the changes in behaviour that they may have caused. Furthermore, some physiological changes might have been an effect, rather than the cause, of fight decisions.

Honest and dishonest displays, motivational state and subsequent decisions in hermit crab shell fights

Animal fights are typically preceded by displays and there is debate whether these are always honest. We investigated the prefight period in hermit crabs, Pagurus bernhardus, during which up to four types of display plus other activities that might provide information are performed. We determined how each display influences or predicts various fight decisions, and related these displays to the motivational state of the attacker, as determined by a startle response, and of the motivational state of the defender, as determined by the duration for which it resisted eviction from its shell. Two displays appeared to have consistent but different effects. Cheliped presentation, where the claws were held in a stationary position, often by both crabs but for longer by the larger, seemed to be honest, and allowed for mutual size assessment. This display enhanced the motivation and the success of the larger crab. In contrast, cheliped extension, involving the rapid thrust of the open chelae towards the opponent, did not seem to allow for mutual size assessment and may contain an element of bluff. It was performed more by the smaller crab and enhanced its success. The complexity of displays in this species appears to allow for both honesty and manipulation.