A systematic review and meta-analysis of unimodal and multimodal predation risk assessment in birds.

Despite a wealth of studies documenting prey responses to perceived predation risk, researchers have only recently begun to consider how prey integrate information from multiple cues in their assessment of risk. We conduct a systematic review and meta-analysis of studies that experimentally manipulated perceived predation risk in birds and evaluate support for three alternative models of cue integration: redundancy/equivalence, enhancement, and antagonism. One key insight from our analysis is that the current theory, generally applied to study cue integration in animals, is incomplete. These theories specify the effects of increasing information level on mean, but not variance, in responses. In contrast, we show that providing multiple complementary cues of predation risk simultaneously does not affect mean response. Instead, as information richness increases, populations appear to assess risk more accurately, resulting in lower among-population variance in response to manipulations of perceived predation risk. We show that this may arise via a statistical process called maximum-likelihood estimation (MLE) integration. Our meta-analysis illustrates how explicit consideration of variance in responses can yield important biological insights.

Information Gathering Is Associated with Increased Survival: A Field Experiment in Black-Capped Chickadees (Poecile atricapillus).

AbstractSampling, investing time or energy to learn about the environment, allows organisms to track changes in resource distribution and quality. The use of sampling is predicted to change as a function of energy expenditure, food availability, and starvation risk, all of which can vary both within and among individuals. We studied sampling behavior in a field study with black-capped chickadees (Poecile atricapillus) and show that individuals adjust their use of sampling as a function of ambient temperature (a proxy for energy expenditure), the presence of an alternative food source (yes or no, a proxy for risk of energy shortfall), and their interaction, as predicted by models of optimal sampling. We also observed repeatable differences in sampling. Some individuals consistently sampled more, and individuals that sampled more overall also had a higher annual survival. These results are consistent with among-individual differences in resource acquisition (e.g., food caches or dominance-related differences in priority access to feeders), shaping among-individual differences in both sampling and survival, with greater resource acquisition leading to both higher sampling and higher survival. Although this explanation requires explicit testing, it is in line with several recent studies suggesting that variation in resource acquisition is a key mechanism underlying animal personality.

Peregrine falcons shift mean and variance in provisioning in response to increasing brood demand.

The hierarchical model of provisioning posits that parents employ a strategic, sequential use of three provisioning tactics as offspring demand increases (e.g., due to increasing brood size and age). Namely, increasing delivery rate (reducing intervals between provisioning visits), expanding provisioned diet breadth, and adopting variance-sensitive provisioning. We evaluated this model in an Arctic breeding population of Peregrine falcons (Falco peregrinus tundrius) by analyzing changes in inter-visit-intervals (IVIs) and residual variance in IVIs across 7 study years. Data were collected using motion-sensitive nest camera images and analyzed using Bayesian mixed effect models. We found strong support for a decrease in IVIs (i.e., increase in delivery rates) between provisioning visits and an increase in residual variance in IVIs with increasing nestling age, consistent with the notion that peregrines shift to variance-prone provisioning strategies with increasing nestling demand. However, support for predictions made based on the hierarchical model of tactics for coping with increased brood demand was equivocal as we did not find evidence in support of expected covariances between random effects (i.e., between IVI to an average sized brood (intercept), change in IVI with brood demand (slope) or variance in IVI). Overall, our study provides important biological insights into how parents cope with increased brood demand.

Does fluctuating selection maintain variation in nest defense behavior in Arctic peregrine falcons (Falco peregrinus tundrius)?

Behavioral expression can vary both within- (i.e., plasticity) and among-individuals (i.e., animal personality), and understanding the causes and consequences of variation at each of these levels is a major area of investigation in contemporary behavioral ecology. Here, we studied sources of variation in both plasticity and personality in nest defense behavior in Arctic peregrine falcons (Falco peregrinus tundrius) in two consecutive years. We found that peregrines adjusted their nest defense in response to nesting stage and year, revealing plastic, state-dependent, adjustment of nest defense. At the same time, nest defense behavior was repeatable in peregrine falcons both within and between years. We tested if fluctuating selection on behavioral types (i.e., individuals average phenotypic expression) and/or assortative mating acted to maintain long-term among-individual differences in nest defense behavior. We found that selection on female nest defense differed across years; being positive in 1 year and negative in the other. We also found support for assortative mating in the first year, but disassortative mating in the second. We propose two potential explanations for the observed year-specific patterns of nonrandom mating: (1) year-specific plastic adjustment of nest defense and/or (2) changes in the age-structure of the breeding population. These posthoc explanations are speculative, and require further study. Unfortunately, we could not evaluate this directly with the available data, and future studies are needed with more than 2 years of data on nest-defense and fitness outcomes, and with a larger number of marked individuals, to properly evaluate these potential explanations.

Individual risk-taking behaviour in black-capped chickadees (Poecile atricapillus) does not predict annual survival.

Within species, individuals often show repeatable differences in behaviours, called 'animal personality'. One behaviour that has been widely studied is how quickly an individual resumes feeding after a disturbance, referred to as boldness or risk-taking. Depending on the mechanism(s) shaping risk-taking behaviour, risk-taking could be positively, negatively, or not associated with differences in overall survival. We studied risk-taking and survival in a population of free-living black-capped chickadees (Poecile atricapillus) in which we previously showed repeatable among-individual differences in risk-taking over the course of several months. We found no evidence that variation in risk-taking is associated with differences in annual survival. We suggest that variation in risk-taking is likely shaped by multiple mechanisms simultaneously, such that the net effect on survival is small or null. For example, among-individual differences in energy demand may favour greater risk-taking without imposing an overall mortality cost if higher energy demand covaries with escape flight performance. We propose directions for future work, including using a multi-trait, multi-year approach to study risk-taking, to allow for stronger inferences regarding the mechanisms shaping these behavioural decisions.

Differences in resource acquisition, not allocation, mediate the relationship between behaviour and fitness: a systematic review and meta-analysis.

Within populations, individuals often show repeatable variation in behaviour, called 'animal personality'. In the last few decades, numerous empirical studies have attempted to elucidate the mechanisms maintaining this variation, such as life-history trade-offs. Theory predicts that among-individual variation in behavioural traits could be maintained if traits that are positively associated with reproduction are simultaneously associated with decreased survival, such that different levels of behavioural expression lead to the same net fitness outcome. However, variation in resource acquisition may also be important in mediating the relationship between individual behaviour and fitness components (survival and reproduction). For example, if certain phenotypes (e.g. dominance or aggressiveness) are associated with higher resource acquisition, those individuals may have both higher reproduction and higher survival, relative to others in the population. When individuals differ in their ability to acquire resources, trade-offs are only expected to be observed at the within-individual level (i.e. for a given amount of resource, if an individual increases its allocation to reproduction, it comes at the cost of allocation to survival, and vice versa), while among individuals traits that are associated with increased survival may also be associated with increased reproduction. We performed a systematic review and meta-analysis, asking: (i) do among-individual differences in behaviour reflect among-individual differences in resource acquisition and/or allocation, and (ii) is the relationship between behaviour and fitness affected by the type of behaviour and the testing environment? Our meta-analysis consisted of 759 estimates from 193 studies. Our meta-analysis revealed a positive correlation between pairs of estimates using both survival and reproduction as fitness proxies. That is, for a given study, behaviours that were associated with increased reproduction were also associated with increased survival, suggesting that variation in behaviour at the among-individual level largely reflects differences among individuals in resource acquisition. Furthermore, we found the same positive correlation between pairs of estimates using both survival and reproduction as fitness proxies at the phenotypic level. This is significant because we also demonstrated that these phenotypic correlations primarily reflect within-individual correlations. Thus, even when accounting for among-individual differences in resource acquisition, we did not find evidence of trade-offs at the within-individual level. Overall, the relationship between behaviour and fitness proxies was not statistically different from zero at the among-individual, phenotypic, and within-individual levels; this relationship was not affected by behavioural category nor by the testing condition. Our meta-analysis highlights that variation in resource acquisition may be more important in driving the relationship between behaviour and fitness than previously thought, including at the within-individual level. We suggest that this may come about via heterogeneity in resource availability or age-related effects, with higher resource availability and/or age leading to state-dependent shifts in behaviour that simultaneously increase both survival and reproduction. We emphasize that future studies examining the mechanisms maintaining behavioural variation in populations should test the link between behavioural expression and resource acquisition - both within and among individuals. Such work will allow the field of animal personality to develop specific predictions regarding the mediating effect of resource acquisition on the fitness consequences of individual behaviour.

No effect of passive integrated transponder tagging method on survival or body condition in a northern population of Black-capped Chickadees (Poecile atricapillus).

Passive integrated transponder (PIT) tags allow a range of individual-level data to be collected passively and have become a commonly used technology in many avian studies. Although the potential adverse effects of PIT tags have been evaluated in several species, explicit investigations of their impacts on small (<12 g) birds are limited. This is important, because it is reasonable to expect that smaller birds could be impacted more strongly by application of PIT tags. In this study, we individually marked Black-capped Chickadees (Poecile atricapillus), a small (circa 10 g) passerine, at the University of Alberta Botanic Garden to evaluate potential lethal and sublethal effects of two PIT tagging methods: attachment to leg bands or subcutaneous implantation. We used a Cox proportional hazards model to compare the apparent survival of chickadees with leg band (N = 79) and implanted PIT tags (N = 77) compared with control birds that received no PIT tags (N = 76) over the subsequent 2 years based on mist net recaptures. We used radio-frequency identification (RFID) redetections of leg band PIT tags to evaluate sex-specific survival and increase the accuracy of our survival estimates. We also used a generalized linear regression model to compare the body condition of birds recaptured after overwintering with leg band PIT tags, implanted PIT tags, or neither. Our analysis found no evidence for adverse effects of either PIT tagging method on survival or body condition. While we recommend carefully monitoring study animals and evaluating the efficacy of different PIT tagging methods, we have shown that both leg band and subcutaneously implanted PIT tags ethical means of obtaining individualized information in a small passerine.

Visual cues of predation risk outweigh acoustic cues: a field experiment in black-capped chickadees.

Foragers rely on various cues to assess predation risk. Information theory predicts that high certainty cues should be valued more than low certainty cues. We measured the latency of black-capped chickadees (Poecile atricapillus) to resume feeding during winter in response to cues that conferred different degrees of certainty about current predation risk: a high certainty visual cue (predator mount) and a lower certainty acoustic cue (conspecific mobbing calls), presented either alone or in combination. As predicted, chickadees took longer to resume feeding after the visual than the acoustic cue, and this effect was greatest under conditions of high starvation risk (i.e. low temperatures). Presenting both cues together produced the same foraging delay as the visual cue alone under low starvation risk, but surprisingly, resulted in lower responses under high starvation risk compared to the visual cue alone. We suggest that this may be due to prey using a form of information updating, whereby differences in the timing of perception of acoustic versus visual cues interacts with energetic constraint to shape perceived risk. Although the sequential perception of cues is likely in a range of decision-making contexts, studies manipulating the order in which cues are perceived are needed to test existing models of multimodal cue integration.

Red knots (Calidris canutus islandica) manage body mass with dieting and activity.

Mass regulation in birds is well documented. For example, birds can increase body mass in response to lower availability and/or predictability of food and decrease body mass in response to increased predation danger. Birds also demonstrate an ability to maintain body mass across a range of food qualities. Although the adaptive significance of mass regulation has received a great deal of theoretical and empirical attention, the mechanisms by which birds achieve this have not. Several non-exclusive mechanisms could facilitate mass regulation in birds. Birds could regulate body mass by adjusting food intake (dieting), activity, baseline energetic requirements (basal metabolic rate), mitochondrial efficiency or assimilation efficiency. Here, we present the results of two experiments in captive red knots (Calidris canutus islandica) that assess three of these proposed mechanisms: dieting, activity and up- and down-regulation of metabolic rate. In the first experiment, knots were exposed to cues of predation risk that led them to exhibit presumably adaptive mass loss. In the second experiment, knots maintained constant body mass despite being fed alternating high- and low-quality diets. In both experiments, regulation of body mass was achieved through a combination of changes in food intake and activity. Both experiments also provide some evidence for a role of metabolic adjustments. Taken together, these two experiments demonstrate that fine-scale management of body mass in knots is achieved through multiple mechanisms acting simultaneously.

Within-Individual Canalization Contributes to Age-Related Increases in Trait Repeatability: A Longitudinal Experiment in Red Knots.

Age-related increases in the repeatable expression of labile phenotypic traits are often assumed to arise from an increase in among-individual variance due to differences in developmental plasticity or by means of state-behavior feedbacks. However, age-related increases in repeatability could also arise from a decrease in within-individual variance as a result of stabilizing trait expression, that is, canalization. Here we describe age-related changes in within-individual and among-individual variance components in two correlated traits-gizzard mass and exploration behavior-in a medium-sized shorebird, the red knot (Calidris canutus). Increased repeatability of gizzard mass came about due to an increase in among-individual variance, unrelated to differences in developmental plasticity, together with decreases in within-individual variance consistent with canalization. We also found canalization of exploration but no age-related increase in overall repeatability, which suggests that showing predictable expression of exploration behavior may be advantageous from a very young age onward. Contrasts between juveniles and adults in the first year after their capture provide support for the idea that environmental conditions play a key role in generating among-individual variation in both gizzard mass and exploration behavior. Our study shows that stabilization of traits occurs under constant conditions: with increased exposure to predictable cues, individuals may become more certain in their assessment of the environment allowing traits to become canalized.

Context is key: A comment on Herczeg et al. 2019.

In the last several years, there has been a surge in the number of studies addressing the causes and consequences of among-individual variation in cognitive ability and behavioural plasticity. Here, we use a recent publication by Herczeg et al. (2019: 32(3), 218-226) to highlight three shortcomings common to this newly emerging field. In their study, Herczeg et al. attempted to link variation in cognitive ability and behavioural plasticity by testing whether selection lines of guppies (Poecilia reticulata) that differ in relative brain size also differ in behavioural plasticity, as might be expected if the costs to plasticity are predominantly derived from the cost of developing large brains. First, residual brain size may not be a suitable proxy for 'cognitive ability'. Recent work has shown that intraspecific variation in cognitive ability can be better understood by considering variation in the specific brain areas responsible for the relevant behaviours as opposed to whole-brain mass. Second, the measure of behavioural plasticity, habituation, is unlikely to fulfil the assumptions that plasticity is both adaptive and costly. Finally, we point out several misconceptions regarding animal personality that continue to contribute to the choice of traits that are not well aligned with study objectives. Elucidating the mechanisms underlying among-individual variation in cognition and behavioural plasticity within populations requires integration between behavioural ecology and comparative cognition, and the study system developed by Herczeg et al. has the potential to provide important mechanistic insights. We hope that by articulating and critically appraising the underlying assumptions that are common in these traditionally separate disciplines, a strong foundation can emerge to allow for more fruitful integration of these fields.

Effects of manipulated levels of predation threat on parental provisioning and nestling begging.

Parental provisioning behavior is a major determinant of offspring growth and survival, but high provisioning rates might come at the cost of increased predation threat. Parents should thus adjust provisioning activity according to current predation threat levels. Moreover, life-history theory predicts that response to predation threat should be correlated with investment in current reproduction. We experimentally manipulated perceived predation threat in free-living great tits (Parus major) by presenting parents with a nest predator model while monitoring different aspects of provisioning behavior and nestling begging. Experiments were conducted in 2 years differing greatly in ecological conditions, including food availability. We further quantified male territorial aggressiveness and male and female exploratory tendency. Parents adjusted provisioning according to current levels of threat in an apparently adaptive way. They delayed nest visits during periods of elevated perceived predation threat and subsequently compensated for lost feeding opportunities by increasing provisioning once the immediate threat had diminished. Nestling begging increased after elevated levels of predation threat, but returned to baseline levels by the end of the experiment, suggesting that parents had fully compensated for lost feeding opportunities. There was no evidence for a link between male exploration behavior or aggressiveness and provisioning behavior. In contrast, fast-exploring females provisioned at higher rates, but only in the year with poor environmental conditions, which might indicate a greater willingness to invest in current reproduction in general. Future work should assess whether these personality-related differences in delivery rates under harsher conditions came at a cost of reduced residual reproductive value.

Evolutionary design of a flexible, seasonally migratory, avian phenotype: why trade gizzard mass against pectoral muscle mass?

Migratory birds undergo impressive body remodelling over the course of an annual cycle. Prior to long-distance flights, red knots ( Calidris canutus islandica) reduce gizzard mass while increasing body mass and pectoral muscle mass. Although body mass and pectoral muscle mass are functionally linked via their joint effects on flight performance, gizzard and pectoral muscle mass are thought to be independently regulated. Current hypotheses for observed negative within-individual covariation between gizzard and pectoral muscle mass in free-living knots are based on a common factor (e.g. migration) simultaneously affecting both traits, and/or protein limitation forcing allocation decisions. We used diet manipulations to generate within-individual variation in gizzard mass and test for independence between gizzard and pectoral muscle mass within individuals outside the period of migration and under conditions of high protein availability. Contrary to our prediction, we observed a negative within-individual covariation between gizzard and pectoral muscle mass. We discuss this result as a potential outcome of an evolved mechanism underlying body remodelling associated with migration. Although our proposed mechanism requires empirical testing, this study echoes earlier calls for greater integration of studies of function and mechanism, and in particular, the need for more explicit consideration of the evolution of mechanisms underlying phenotypic design.

Facultative parasites as evolutionary stepping-stones towards parasitic lifestyles.

Parasites and parasitic lifestyles have evolved from free-living organisms multiple times. How such a key evolutionary transition occurred remains puzzling. Facultative parasites represent potential transitional states between free-living and fully parasitic lifestyles because they can be either free-living or parasitic depending on environmental conditions. We suggest that facultative parasites with phenotypically plastic life-history strategies may serve as evolutionary stepping-stones towards obligate parasitism. Pre-adaptations provide a starting point for the transition towards opportunistic or facultative parasitism, but what evolutionary mechanism underlies the transition from facultative to obligate parasitism? In this Opinion Piece, we outline how facultative parasites could evolve towards obligate parasites via genetic assimilation, either alone or in combination with the Baldwin effect. We further describe the key predictions stemming from each of these evolutionary pathways. The importance of genetic assimilation in evolution has been hotly debated. Studies on facultative parasites may not only provide key insights regarding the evolution of parasitism, but also provide ideal systems in which to test evolutionary theory on genetic accommodation.

The covariance between metabolic rate and behaviour varies across behaviours and thermal types: meta-analytic insights.

Energy metabolism has received much attention as a potential driver of repeatable among-individual differences in behaviour (animal personality). Several factors have been hypothesized to mediate this relationship. We performed a systematic review with a meta-analysis of >70 studies comprised of >8000 individuals reporting relationships between measures of maintenance metabolic rates (i.e. basal metabolic rate, resting metabolic rate, and standard metabolic rate) and behaviour. We evaluated support for three hypothesized mediators: (i) type of behaviour, (ii) opportunities for energy re-allocation, and (iii) magnitude of energetic constraints. Relationships between measures of maintenance metabolic rate (MR) and behaviour are predicted to be strongest for behaviours with strong consequences for energy turnover (acquisition or expenditure). Consistent with this, we found that behaviours with known consequences for energy gain (e.g. foraging, dominance, boldness) or expenditure (e.g. maximum sprint speed, sustained running speed, maximum distance travelled, etc.) had strong positive correlations with MR, while behaviours with putatively weak and/or inconsistent associations with net energy gain or loss (e.g. exploration, activity, sociability) were not correlated with MR. Greater opportunities for energy reallocation are predicted to weaken relationships between MR and behaviour by creating alternative pathways to balance energy budgets. We tested this by contrasting relationships between MR and behaviour in ectotherms versus endotherms, as thermoregulation in endotherms creates additional opportunities for energy reallocation compared with ectotherms. As predicted, the relationship between behaviour and MR was stronger in ectotherms compared with endotherms. However, statistical analyses of heterogeneity among effect sizes from different species did not support energy re-allocation as the main driver of these differences. Finally, we tested whether conditions where animals face greater constraints in meeting their energy budgets (e.g. field versus laboratory, breeding versus non-breeding) increased the strength of the relationship between MR and behaviour. We found that the relationship between MR and behaviour was unaffected by either of these modifiers. This meta-analysis provides two key insights. First, we observed positive relationships of similar magnitude between MR and behaviours that bring in net energy, and behaviours that cost net energy. This result is only consistent with a performance energy-management model. Given that the studies included in our meta-analysis represent a wide range of taxa, this suggests that the performance model may be the most common model in general. Second, we found that behaviours with putatively weak or inconsistent consequences for net energy gain or expenditure (exploration, activity, sociability) show no relationship with MR. The lack of relationship between MR and behavioural traits with weak and/or inconsistent consequences for energy turnover provides the first systematic demonstration of the central importance of the ecological function of traits in mediating relationships between MR and behaviour.

To eat and not be eaten: diurnal mass gain and foraging strategies in wintering great tits.

Adaptive theory predicts that the fundamental trade-off between starvation and predation risk shapes diurnal patterns in foraging activity and mass gain in wintering passerine birds. Foragers mitigating both types of risk should exhibit a bimodal distribution (increased foraging and mass gain early and late in the day), whereas both foraging and mass gains early (versus late) during the day are expected when the risk of starvation (versus predation) is greatest. Finally, relatively constant rates of foraging and mass gain should occur when the starvation-predation risk trade-off is independent of body mass. Using automated feeders with integrated digital balances, we estimated diurnal patterns in foraging and body mass gain to test which ecological scenario was best supported in wintering great tits Parus major Based on data of 40 consecutive winter days recording over 12 000 body masses of 28 individuals, we concluded that birds foraged and gained mass early during the day, as predicted by theory when the starvation-predation risk trade-off is mass-dependent and starvation risk outweighs predation risk. Slower explorers visited the feeders more often, and decreased their activity along the day more strongly, compared with faster explorers, thereby explaining a major portion of the individual differences in diurnal patterning of foraging activity detected using random regression analyses. Birds did not differ in body mass gain trajectories, implying both that individuals differed in the usage of feeders, and that unbiased conclusions regarding how birds resolve starvation-predation risk trade-off require the simultaneous recording of foraging activity and body mass gain trajectories. Our study thereby provides the first unambiguous demonstration that individual birds are capable of adjusting their diurnal foraging and mass gain trajectories in response to ecological predictors of starvation risk as predicted by starvation-predation risk trade-off theory.

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.

Do great tits (Parus major) suppress basal metabolic rate in response to increased perceived predation danger? A field experiment.

Several studies have shown that individuals with higher metabolic rates (MRs) feed at higher rates and are more willing to forage in the presence of predators. This increases the acquisition of resources, which in turn, may help to sustain a higher MR. Elevated predation danger may be expected to result in reduced MRs, either as a means of allowing for reduced feeding and risk-taking, or as a consequence of adaptively reducing intake rates via reduced feeding and/or risk-taking. We tested this prediction in free-living great tits (Parus major) using a playback experiment to manipulate perceived predation danger. There was evidence that changes in body mass and BMR differed as a function of treatment. In predator treatment plots, great tits tended to reduce their body mass, a commonly observed response in birds to increased predation danger. In contrast, birds from control treatment plots showed no overall changes in body mass. There was also evidence that great tits from control treatment plots increased their basal metabolic rate (BMR) over the course of the experiment, presumably due to decreasing ambient temperatures over the study period. However, there was no evidence for changes in BMR for birds from predator treatment plots. Although the directions of these results are consistent with the predicted directions of effects, the effects sizes and confidence intervals yield inconclusive support for the hypothesis that great tits would adaptively suppress BMR in response to increased perceived predation risk. The effect size observed in the present study was small (~1%) and would not be expected to result in substantive reductions in feeding rate and/or risk-taking. Whether or not ecological conditions that generate greater energetic stress (e.g. lower food availability, lower ambient temperatures) could produce an effect that produces biologically meaningful reductions in feeding activity and/or risk-taking remains an open question.

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.