Kimberley J. Mathot

Animal personality and state–behaviour feedbacks: a review and guide for empiricists

An exciting area in behavioural ecology focuses on understanding why animals exhibit consistent among-individual differences in behaviour (animal personalities). Animal personality has been proposed to emerge as an adaptation to individual differences in state variables, leading to the question of why individuals differ consistently in state. Recent theory emphasizes the role that positive feedbacks between state and behaviour can play in producing consistent among-individual covariance between state and behaviour, hence state-dependent personality. We review the role of feedbacks in recent models of adaptive personalities, and provide guidelines for empirical testing of model assumptions and predictions. We discuss the importance of the mediating effects of ecology on these feedbacks, and provide a roadmap for including state-behaviour feedbacks in behavioural ecology research.

Energetics and behavior: unrequited needs and new directions

The number of studies investigating links between among-individual differences in metabolic rate (MR) and behavior has grown dramatically in the past several years. A major and often untested assumption of these studies is that the selected measure of MR is a valid proxy for energetic constraints. We argue that without explicitly testing this assumption, observed patterns between MR and behavior are uninterpretable. We provide guidelines for evaluating how a given measure of MR relates to constraints on the acquisition or expenditure of energy. The approach we advocate will allow researchers to develop and test a priori predictions relating energy metabolism and behavior. We conclude by highlighting several exciting directions for future work in this rapidly growing field.

Disentangling the roles of frequency-vs. state-dependence in generating individual differences in behavioural plasticity

Theoretical work suggests that both negative frequency-dependent payoffs and state-dependent payoffs can lead to individual variation in behavioural plasticity. We investigated the roles of both frequency- and state-dependence on the occurrence of individual variation in behavioural plasticity in a series of experiments where we manipulated perceived predation danger for red knots (Calidris canutus islandica). We found individual variation in plasticity in a trait with negative frequency-dependent payoffs (vigilance), but not in a trait with positive frequency-dependent payoffs (escape flights). Furthermore, there was no correlation between the average level of vigilance under low predation danger and the magnitude of response to increased predation danger, as would be expected under state-dependence. Thus, our results provide support for the hypothesis that negative-frequency dependence favours individual variation in plasticity. However, negative-frequency dependence alone cannot explain why plasticity would be consistent within individuals, and future studies should address the factors that might favour individual consistency.

Does metabolic rate predict risk-taking behaviour?: A field experiment in a wild passerine bird

Summary Individuals often show consistent differences in risk-taking behaviours; behaviours that increase resource acquisition at the expense of an increased risk of mortality. Recently, basal metabolic rate (BMR) has been suggested as a potentially important state variable underlying adaptive individual differences in a range of behaviours, including risk-taking. We tested the relationship between BMR and risk-taking in free-living great tits (Parus major) using experimental manipulations of perceived predation risk. We compared the latency of individuals to return to feeders following control (human) and predator (model sparrowhawk, Accipiter nisus) disturbances at fixed feeder locations. We predicted that if variation in risk-taking is shaped by energetic constraints, high BMR individuals should return to feeders sooner following both disturbance types and show smaller changes in risk-taking as a function of predation danger. Higher BMR tended to be associated with lower risk-taking following control disturbances but greater risk-taking following predator disturbances, resulting in a significant interaction between BMR and treatment. Within-individual changes in risk-taking as a function of ambient temperature (a proxy for within-individual changes in energetic constraints) mirrored these results. Lower temperatures tended to be associated with lower risk-taking following control disturbances, but greater risk-taking following predator disturbances, resulting in a significant interaction between temperature and treatment. The effects of BMR and temperature on variation in risk-taking as a function of perceived predation danger were qualitatively similar, suggesting that energetic constraints play a role in shaping risk-taking. However, the hypothesized mechanism (energetic requirements directly influence the optimal expression of risk-taking behaviour) is insufficient to account for the observed negative relationship between energetic constraint and risk-taking following control disturbances. We conclude that variation in risk-taking is associated with differences in energetic constraints, including BMR and temperature, but that the relationship is context-specific, here high vs. low perceived predation risk. Further studies are needed to elucidate potential mechanisms that could generate context-specific relationships between energetic constraints and risk-taking.

An approach to estimate short-term, long-term, and reaction norm repeatability

Evolutionary ecologists increasingly study reaction norms that are expressed repeatedly within the same individuals lifetime. For example, foragers continuously alter anti-predator vigilance in response to moment-to-moment changes in predation risk. Variation in this form of plasticity occurs both among and within individuals. Among-individual variation in plasticity (individual by environment interaction or I × E) is commonly studied; by contrast, despite increasing interest in its evolution and ecology, within-individual variation in phenotypic plasticity is not. We outline a study design based on repeated measures and a multilevel extension of random regression models that enables quantification of variation in reaction norms at different hierarchical levels (such as among and within individuals). The approach enables the calculation of repeatability of reaction norm intercepts (average phenotype) and slopes (level of phenotypic plasticity); these indices are not specific to measurement or scaling and are readily comparable across data sets. The proposed study design also enables calculation of repeatability at different temporal scales (such as short- and long-term repeatability), thereby answering calls for the development of approaches enabling scale-dependent repeatability calculations. We introduce a simulation package in the R statistical language to assess power, imprecision and bias for multilevel random regression that may be utilised for realistic data sets (unequal sample sizes across individuals, missing data, etc). We apply the idea to a worked example to illustrate its utility. We conclude that consideration of multilevel variation in reaction norms deepens our understanding of the hierarchical structuring of labile characters and helps reveal the biology in heterogeneous patterns of within-individual variance that would otherwise remain ‘unexplained’ residual variance.

Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.

Sediment in Stomach Contents of Western Sandpipers and Dunlin Provide Evidence of Biofilm Feeding

Abstract. Western Sandpipers and Dunlin are capable of grazing biofilm. As there has been no assessment of this dietary constituent in stomach contents, the stomachs of 89 Western Sandpipers and 56 Dunlin collected during breeding migration through the Fraser River delta, British Columbia, Canada, were examined. Invertebrates, traditionally regarded as the principal prey, comprised a minor fraction of mean stomach volumes (Dunlin: <25%; Western Sandpiper <10%). Three phyla accounted for most of these invertebrates: molluscs, annelids and arthropods. In comparison, sediment (a mixture of sediment particles, broken and unbroken diatoms plus organic detritus) comprised the major component of stomach volumes (Dunlin: >40%; Western Sandpipers: >75%). Although the mean volume of sediment was significantly greater in Western Sandpipers than Dunlin, there was no effect of sex for either species. Stomach sediment volume appears a convenient index of biofilm intake and sediment loads indicative of biofilm grazing have been reported in stomach contents from other shorebird species. Re-examination of shorebird diets appears necessary given that conditions promoting biofilm are not necessarily conducive for invertebrate prey.

Metabolic Rates Can Drive Individual Differences in Information and Insurance Use under the Risk of Starvation

Variation in how individuals invest in acquiring information (sampling) and in insuring themselves against potential negative consequences of uncertainty (e.g., by storing energy reserves) has been suggested to underlie consistent individual differences in suites of behavioral traits. However, the key drivers of individual differences in information use remain poorly understood. We use dynamic programming to explore how existing variation in metabolic rates (MRs) affects the use of sampling and insurance under starvation risk. Our analysis reveals nonlinear effects of MRs on diurnal patterns of sampling and insurance. Individuals with low MRs accrue reserves quickly, because they invest in sampling and are able to exploit profitable options when they arise. Individuals with intermediate MRs initially lose reserves, because sampling, while optimal, is relatively expensive; however, they later build reserves due to efficient exploitation of alternative foraging options. Sampling rarely pays for individuals with the highest MRs, which show relatively constant levels of energy reserves throughout the foraging period. Thus, individual variation in MRs on the scale observed in natural populations can lead to important differences in investment in sampling and insurance and may underpin consistent individual differences in suites of other behavioral traits, including individual differences in behavioral responsiveness.

Basal metabolic rate can evolve independently of morphological and behavioural traits.

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h2=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.

Sources of (co)variation in alternative siring routes available to male great tits (Parus major)

Males of socially monogamous species can increase their siring success via within‐pair and extra‐pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five‐year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as “interactive phenotypes” arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra‐pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra‐pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.