Individual differences in plasticity and sampling when playing behavioural games

When engaged in behavioural games, animals can adjust their use of alternative tactics until groups reach stable equilibria. Recent theory on behavioural plasticity in games predicts that individuals should differ in their plasticity or responsiveness and hence in their degree of behavioural adjustment. Moreover, individuals are predicted to be consistent in their plasticity within and across biological contexts. These predictions have yet to be tested empirically and so we examine the behavioural adjustment of individual nutmeg mannikins (Lonchura punctulata), gregarious ground-feeding passerines, when playing two different social foraging games: producer-scrounger (PS) and patch-choice (PC) games. We found: (i) significant individual differences in plasticity and sampling behaviour in each of the two games, (ii) individual differences in sampling behaviour were consistent over different test conditions within a game (PC) and over a six month period (PS), (iii) but neither individual plasticity nor sampling behaviour was correlated from one social foraging game to another. The rate at which birds sampled alternative tactics was positively associated with seed intake in PS trials but negatively associated in PC trials. These results suggest that games with frequency dependence of pay-offs can maintain differences in behavioural plasticity but that an important component of this plasticity is group- and/or context-specific.     

Intragroup competition predicts individual foraging specialisation in a group‐living mammal

Individual foraging specialisation has important ecological implications, but its causes in group‐living species are unclear. One of the major consequences of group living is increased intragroup competition for resources. Foraging theory predicts that with increased competition, individuals should add new prey items to their diet, widening their foraging niche (‘optimal foraging hypothesis’). However, classic competition theory suggests the opposite: that increased competition leads to niche partitioning and greater individual foraging specialisation (‘niche partitioning hypothesis’). We tested these opposing predictions in wild, group‐living banded mongooses (Mungos mungo), using stable isotope analysis of banded mongoose whiskers to quantify individual and group foraging niche. Individual foraging niche size declined with increasing group size, despite all groups having a similar overall niche size. Our findings support the prediction that competition promotes niche partitioning within social groups and suggest that individual foraging specialisation may play an important role in the formation of stable social groupings.     

Individual differences in foraging site fidelity are not related to time-activity budgets in Herring Gulls

Many populations consist of individuals that differ consistently in their foraging behaviour through resource or foraging site selection. Foraging site fidelity has been reported in several seabird species as a common phenomenon. It is considered especially beneficial in spatially and/or temporally predictable environments in which fidelity is thought to increase energy intake, thereby affecting time-energy budgets. However, the consequences for activity and energy budget have not been adequately tested. In this paper, we studied the consequences of fine-scale foraging site fidelity in adult Herring Gulls Larus argentatus in a highly predictable foraging environment with distinct foraging patches. We measured their time-activity budgets using GPS tracking and tri-axial acceleration measurements, which also made it possible to estimate energy expenditure. Individual variation in foraging site fidelity was high, some individuals spending most of their time on a single foraging patch and others spending the same amount of time in up to 21 patches. While time and activity budgets differed between individuals, we found no clear relationship with foraging site fidelity. We did find a relationship between the size of the birds and the level of site fidelity; faithful birds tend to have a larger body size. Although differences in foraging time and habitat use between individuals could play a role in the results of the current study, short-term consequences of variation in foraging site fidelity within a population remain elusive, even when focusing on individuals with a similar foraging specialization (Blue Mussels Mytilus edulis). Studying individuals over multiple years and under varying environmental conditions may provide better insight into the consequences and plasticity of foraging site fidelity.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

Effects of inbreeding on behavioural plasticity of parent–offspring interactions in a burying beetle

Inbreeding depression is defined as a fitness decline in progeny resulting from mating between related individuals, the severity of which may vary across environmental conditions. Such inbreeding‐by‐environment interactions might reflect that inbred individuals have a lower capacity for adjusting their phenotype to match different environmental conditions better, as shown in prior studies on developmental plasticity. Behavioural plasticity is more flexible than developmental plasticity because it is reversible and relatively quick, but little is known about its sensitivity to inbreeding. Here, we investigate effects of inbreeding on behavioural plasticity in the context of parent–offspring interactions in the burying beetle Nicrophorus vespilloides. Larvae increase begging with the level of hunger, and parents increase their level of care when brood sizes increase. Here, we find that inbreeding increased behavioural plasticity in larvae: inbred larvae reduced their time spent associating with a parent in response to the length of food deprivation more than outbred larvae. However, inbreeding had no effect on the behavioural plasticity of offspring begging or any parental behaviour. Overall, our results show that inbreeding can increase behavioural plasticity. We suggest that inbreeding‐by‐environment interactions might arise when inbreeding is associated with too little or too much plasticity in response to changing environmental conditions.     

Behavioural ecology in traditional societies

Can models from behavioural ecology explain cultural diversity in human populations? Studies of variation in reproductive and productive behaviour, both within and between traditional societies, are beginning to show that specific predictions from sexual selection and optimal foraging theory can be developed and tested with human data. Greatest success has been in the study of foraging; whereas attempts to understand patterns of marriage and parental investment have been most convincing in those cases where behaviour is related to specific ecological and social conditions. The aim of human behavioural ecologists in the future will be to determine the constraints that the dual goals of reproduction and production place on individuals.     

Nonadditive effects of group membership can lead to additive group phenotypes for anti-predator behaviour of guppies, Poecilia reticulata

Nonadditive effects of group membership are generated when individuals respond differently to the same social environment and may alter predictions about how behavioural evolution will occur. Despite this importance, the relationship between an individual's behaviour in two different social contexts and how reciprocal interactions among individuals within groups influence group behaviour are poorly understood. Guppy anti-predator behaviour can be used to explore how individuals behaviourally respond to changes in social context. Individuals from two strains were tested for response to a model predator alone and in groups to evaluate how individuals alter their behaviour in response to social context and how group phenotype relates to individual behaviour. Nonadditive effects of group membership were detected for a number of behaviours, revealing that the effect of being in a group differed among individuals. These nonadditive effects, however, yielded an additive group phenotype. That is, the average behaviour of the group was equal to the average of its parts, for all behaviours in both strains. Such an additive group phenotype may have resulted because all individuals within a group respond to the specific social environment provided by the other members of their group.     

Behavioural plasticity in a native species may be related to foraging resilience in the presence of an aggressive invader

Competition between invasive and native species can result in the exploitation of resources by the invader, reducing foraging rates of natives. However, it is increasingly recognized that multiple factors can enhance the resilience of native species competing for limiting resources with invaders. Although extensively studied in terrestrial species, little research has focused on behavioural plasticity in aquatic ecosystems and how this influences native species resilience. Here, we examined the role of behavioural plasticity in interactions between a native Australian fish, Pseudomugil signifer, and a widespread invasive fish, Gambusia holbrooki. To determine whether P. signifer displays behavioural plasticity that may mitigate competition with G. holbrooki, we first quantified social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups. Second, we compared the feeding rates of both species in these groups to ascertain if any modulation of social behaviours and cohesion related to foraging success. We found that aggressive and submissive behaviours of G. holbrooki and P. signifer showed plasticity in the presence of heterospecifics, but social affiliation, shoaling and, most importantly, foraging, remained inflexible. This variation in the degree of plasticity highlights the complexity of the behavioural response of a native species and suggests that both behavioural modulation and consistency may be related to sustaining foraging efficiency in the presence of an invader.     

Social effects on foraging behavior and success depend on local environmental conditions

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5‐month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low‐ranked individuals received more agonism, but this only translated into reduced foraging performances for low‐ranked individuals in the high‐competition experimental conditions. Our results suggest one possible reason for this pattern may be low‐ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank‐offsetting effect of this investment being overwhelmed in the higher‐competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.     

Variation in personality and behavioural plasticity across four populations of the great tit Parus major

1. Interest in the evolutionary origin and maintenance of individual behavioural variation and behavioural plasticity has increased in recent years. 2. Consistent individual behavioural differences imply limited behavioural plasticity, but the proximate causes and wider consequences of this potential constraint remain poorly understood. To date, few attempts have been made to explore whether individual variation in behavioural plasticity exists, either within or between populations. 3. We assayed 'exploration behaviour' among wild-caught individual great tits Parus major when exposed to a novel environment room in four populations across Europe. We quantified levels of individual variation within and between populations in average behaviour, and in behavioural plasticity with respect to (i) repeated exposure to the room (test sequence), (ii) the time of year in which the assays were conducted and (iii) the interval between successive tests, all of which indicate habituation to novelty and are therefore of functional significance. 4. Consistent individual differences ('I') in behaviour were present in all populations; repeatability (range: 0.34-0.42) did not vary between populations. Exploration behaviour was also plastic, increasing with test sequence - but less so when the interval between subsequent tests was relatively large - and time of year; populations differed in the magnitude of plasticity with respect to time of year and test interval. Finally, the between-individual variance in exploration behaviour increased significantly from first to repeat tests in all populations. Individuals with high initial scores showed greater increases in exploration score than individuals with low initial scores; individual by environment interaction ('I × E') with respect to test sequence did not vary between populations. 5. Our findings imply that individual variation in both average level of behaviour and behavioural plasticity may generally characterize wild great tit populations and may largely be shaped by mechanisms acting within populations. Experimental approaches are now needed to confirm that individual differences in behavioural plasticity (habituation) - not other hidden biological factors - caused the observed patterns of I × E. Establishing the evolutionary causes and consequences of this variation in habituation to novelty constitutes an exciting future challenge.     

Unequal competitor ideal free distribution in fish?

Key predictions of unequal competitor ideal free distribution models were tested using a continuous input situation. Ten individually identifiable cichlid fish competed for food items at either end of their tank. Their distribution fitted the predictions of the equal competitor, continuous input ideal free model almost perfectly. However, examination of individual intakes revealed significant variation in individual success and relative competitive ability between patches. Contrary to expectations, fish did not exclusively use the patch where their intake was higher, although individuals experiencing greater differences in intake rate between patches were more selective. We found no evidence for a truncated distribution or even a correlation between competitive ability and patch quality. Changing the input regime to reduce competition did not produce a decrease in the range of intake rates between individuals. This study indicates the value of future empirical and theoretical work on how relative competitive ability varies with the nature of the foraging environment.     

Boldness and Information Use in Three‐Spined Sticklebacks

In foraging groups, individuals may utilise information from their social environment to aid decision making when choosing where to search for food. Little work has looked at the costs or benefits of behavioural differences, such as consistent individual variation in boldness, with respect to learning ability. Here, we investigate the response of three‐spined stickleback (Gasterosteus aculeatus) to ‘social cues’, ‘local enhancement’ and ‘public information’ during foraging tasks. Our results confirm previous work suggesting that this species responds to social cues and local enhancement but not public information. Variation in boldness did not affect the use of different types of information. However, time taken to make a choice and reach a patch varied between fish with different levels of boldness. Contrary to expectation, shy fish were the more variable individuals, having a greater range of reaction times when responding to the tasks. This suggests that individual behavioural differences still play a role when utilising information obtained from the environment and may influence the relative benefits that could result in different contexts.     

Individual foraging specialisation in a social mammal: the European badger (Meles meles)

Individual specialisation has been identified in an increasing number of animal species and populations. However, in some groups, such as terrestrial mammals, it is difficult to disentangle individual niche variation from spatial variation in resource availability. In the present study, we investigate individual variation in the foraging niche of the European badger (Meles meles), a social carnivore that lives in a shared group territory, but forages predominantly alone. Using stable isotope analysis, we distinguish the extent to which foraging variation in badgers is determined by social and spatial constraints and by individual differences within groups. We found a tendency for individual badgers within groups to differ markedly and consistently in their isotope values, suggesting that individuals living with access to the same resources occupied distinctive foraging niches. Although sex had a significant effect on isotope values, substantial variation within groups occurred independently of age and sex. Individual differences were consistent over a period of several months and in some instances were highly consistent across the two years of the study, suggesting long-term individual foraging specialisations. Individual specialisation in foraging may, therefore, persist in populations of territorial species not solely as a result of spatial variation in resources, but also arising from individuals selecting differently from the same available resources. Although the exact cause of this behaviour is unknown, we suggest that specialisation may occur due to learning trade-offs which may limit individual niche widths. However, ecological factors at the group level, such as competition, may also influence the degree of specialisation.     

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.     

Effects of body mass on the foraging behaviour of subordinate Coal Tits Parus ater

Several mechanisms can explain individual differences in foraging behaviour, such as variation in predation risk between patches, variation in the ability of individuals to detect or escape from predators, variation between individuals in their requirement for food, the quality and abundance of food in different patches, phenotypic variation giving rise to differences in resource use (exploitation hypothesis) and interference competition such as the exclusion of subordinate individuals by dominants. Subordinates can develop compensation mechanisms. One of these mechanisms is morphological differentiation. However not every change in morphology can account for the same variation in behaviour, since some morphologies can be ecologically more plastic than others (i.e. some morphs can exploit a broader niche than other morphs). Under controlled conditions in the Coal Tit Parus ater, we tested whether (1) differences in resource use were explained by either the exploitation hypothesis or by the interference hypothesis, and (2) the presumed costs of subordination can be reduced through different ecological plasticities associated with different morphologies. Our results support the interference hypothesis as there are no differences in hanging behaviour between dominants and subordinates when foraging solitarily; while in the presence of other individuals, we observed differences in foraging behaviour that varied with social status. Our results also show that body mass influenced foraging behaviour; lighter birds can exploit patches where hanging postures are needed more easily than heavier birds. Moreover, this relationship varied among individuals, as predicted by the ecological plasticity hypothesis. Lighter subordinate individuals used hanging postures more frequently than heavier ones, differentially reducing the costs of subordination. We propose that differences in the breadth of ecological niche due to differences in morphology can reduce the costs of subordination.     

How host plant variability influences the advantages to learning: a theoretical model for oviposition behaviour in Lepidoptera

Learning can allow individuals to increase their fitness in particular environments. The advantage to learning depends on the predictability of the environment and the extent to which animals can adjust their behaviour. Earlier general models have investigated when environmental predictability might favour the evolution of learning in foraging animals. Here, we construct a theoretical model that predicts the advantages to learning using a specific biological example: oviposition in the Lepidoptera. Our model includes environmental and behavioural complexities relevant to host selection in these insects and tests whether the predictions of the general models still hold. Our results demonstrate how the advantage of learning is maximised when within-generation variability is minimised (the local environment consists mainly of a single host plant species) and between-generation variability is maximised (different host plant species are the most common in different generations). We discuss how our results: (a) can be applied to recent empirical work in different lepidopteran species and (b) predict an important role of learning in lepidopteran agricultural pests.     

Individual and Sex Differences in Habituation and Neophobia in House Sparrows (Passer domesticus)

Heterogeneity in the environment favours foragers that are flexible (phenotypically plastic). However, consistent individual differences in behaviour (personality), such as in risk‐taking, might affect an individual's ability to find food, avoid predators and adjust to new conditions. It is now well known that personalities exist in many taxa, but much less is known about individual variation in plasticity. We measured the tendency to begin foraging across different levels of risk in house sparrows (Passer domesticus), using a behavioural reaction norm framework to simultaneously assess personality and plasticity. We asked whether individuals were consistently different across risk levels, and whether they differed in habituation and neophobia, both of which were treated as cases of plasticity. We found that males habituated more than females by beginning to feed sooner after repeated instances of a human disturbance in the presence of an initially unfamiliar object. Individuals of both sexes also exhibited consistent differences across trials, but did not differ in the rate of habituation beyond the difference between the sexes. When a novel object was placed in the foraging area, both sexes exhibited similar degrees of neophobia by delaying feeding. The magnitude of this change varied among birds, indicating individual differences in neophobia. Our results indicate that both personality and individual variation in plasticity exist but should be treated as independent phenomena. The presence of variation in plasticity implies that the raw material necessary for selection on neophobia exists, and that if heritable, plasticity in risk‐taking across contexts could evolve.     

Individual plastic responses by males to rivals reveal mismatches between behaviour and fitness outcomes

Plasticity in behaviour is of fundamental significance when environments are variable. Such plasticity is particularly important in the context of rapid changes in the socio-sexual environment. Males can exhibit adaptive plastic responses to variation in the overall level of reproductive competition. However, the extent of behavioural flexibility within individuals, and the degree to which rapidly changing plastic responses map onto fitness are unknown. We addressed this by determining the behaviour and fitness profiles of individual Drosophila melanogaster males subjected to up to three episodes of exposure to rivals or no rivals, in all combinations. Behaviour (mating duration) was remarkably sensitive to the level of competition and fully reversible, suggesting that substantial costs arise from the incorrect expression of even highly flexible behaviour. However, changes in mating duration matched fitness outcomes (offspring number) only in scenarios in which males experienced zero then high competition. Following the removal of competition, mating duration, but not offspring production, decreased to below control levels. This indicates that the benefit of increasing reproductive investment when encountering rivals may exceed that of decreasing investment when rivals disappear. Such asymmetric fitness benefits and mismatches with behavioural responses are expected to exert strong selection on the evolution of plasticity.     

Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly

We investigated four predictions about how temperature, photoperiod and sex affect the life history plasticity and foraging activity of a damselfly. (i) As predicted, increased temperatures increased foraging activity and growth rates, but in contrast with the prediction, late photoperiod (high time stress) did not affect foraging activity and growth rate. (ii) Unexpectedly, the increase in growth rate at increasing temperatures was not larger under high time stress. (iii) As predicted, age and size at emergence decreased at higher temperatures and at the late photoperiod. Temperature-induced life history shifts were direct or the result of behavioural growth mediation depending on the temperature range. Photoperiod-induced life history shifts were direct. (iv) As predicted, males emerged before females but at a smaller size. The degree of sexual size dimorphism was influenced by the joint effects of temperature and photoperiod. We could only detect genetic variation in size plasticity to photoperiod. The match between the sex-specific life history responses to temperature and photoperiod and predictions by relevant optimality models suggests adaptive life history plasticity to these variables.