Bigger is not always better: Viability selection on body mass varies across life stages in a hibernating mammal

Body mass is often viewed as a proxy of past access to resources and of future survival and reproductive success. Links between body mass and survival or reproduction are, however, likely to differ between age classes and sexes. Remarkably, this is rarely taken into account in selection analyses. Selection on body mass is likely to be the primary target accounting for juvenile survival until reproduction but may weaken after recruitment. Males and females also often differ in how they use resources for reproduction and survival. Using a long‐term study on body mass and annual survival in yellow‐bellied marmots (Marmota flaviventer), we show that body mass was under stabilizing viability selection in the first years of life, before recruitment, which changed to positive directional selection as age increased and animals matured. We found no evidence that viability selection across age classes on body mass differed between sexes. By investigating the link between running speed and body mass, we show that the capacity to escape predators was not consistent across age classes and followed a quadratic relationship at young ages only. Overall, our results indicate that mature age classes exhibit traditional patterns of positive viability selection on body mass, as expected in a hibernating mammal, but that mass in the first years of life is subjected to stabilizing selection which may come from additional predation pressures that negate the benefits of the largest body masses. Our study highlights the importance to disentangle selection pressures on traits across critical age (or life) classes.     

Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk?

Abstract Different body components are thought to trade off in their growth and development rates, but the causes for relative prioritization of any trait remains a critical question. Offspring of species at higher risk of predation might prioritize development of locomotor traits that facilitate escaping risky environments over growth of mass. We tested this possibility in 12 altricial passerine species that differed in their risk of nest predation. We found that rates of growth and development of mass, wings, and endothermy increased with nest predation risk across species. In particular, species with higher nest predation risk exhibited relatively faster growth of wings than of mass, fledged with relatively larger wing sizes and smaller mass, and developed endothermy earlier at relatively smaller mass. This differential development can facilitate both escape from predators and survival outside of the nest environment. Tarsus growth was not differentially prioritized with respect to nest predation risk, and instead all species achieved adult tarsus size by age of fledging. We also tested whether different foraging modes (aerial, arboreal, and ground foragers) might explain the variation of differential growth of locomotor modules, but we found that little residual variation was explained. Our results suggest that differences in nest predation risk among species are associated with relative prioritization of body components to facilitate escape from the risky nest environment.     

Mass-dependence in the predation risk of unequal competitors; some models

Foragers can monitor their survival through the size of body reserves in a starvation/predation risk trade-off. Energy reserves reduce the risk of energetic shortfall, while survival will be maximised at intermediate reserve levels when there is a cost of carrying mass loads. The size of reserves that will maximise survival may not be identical for unequal competitors, when unequal access to resources will affect the costs and benefits of energy reserves. Here, I evaluate the effect of competitive ability (dominance) for the mass-dependence in predation risk and how it is affected by (1) attack rate (attack rate effect), (2) distance to the emergence of an unconcealed predator attack (attack distance effect) and (3) distance to cover (cover distance effect). This general model is illustrated by empirical data for parameters specific for birds. The effect of competitive ability for the mass-dependence in predation risk is ambiguous and depends on how rank is mediated into mass-dependent predation risk. Dominants pay a lower cost in predation risk for mass loads than sub-ordinates when competitive ability entails that they feed closer to cover (cover distance effect) and when the exposure to attacks and attack rate is lower than for sub-ordinates (attack rate effect) . In contrast, a shorter distance to the emergence of an unconcealed attack (attack distance effect) implies a lower increase in predation risk with mass for sub-ordinates. As a consequence of how the cost of mass load varies with conditions there is no unambiguous relationship for how predation risk can be traded off for starvation risk for individuals with different competitive ability.     

Maternal effects across life stages: larvae experiencing predation risk increase offspring provisioning

1. Maternal provisioning can reduce offspring vulnerability to predators by promoting offspring growth and eliciting of antipredator behaviours. Mothers perceiving predation risk may improve offspring survival if producing larger, higher‐quality offspring. However, empirical evidence suggests that offspring quality is often reduced, probably reflecting predator‐induced physiological costs, or a selfish maternal strategy aimed at producing more offspring by sacrificing their quality. While perception and impact of predators can vary across the prey's life stage, a majority of studies have focused on understanding how reproductive allocation decisions are influenced by the risk of predation during adulthood. 2. In this study, Leptinotarsa decemlineata beetles were used to examine if the risk of predation during the larval stage: (i) impacts the mother's physiological condition, including body mass and metabolic rate; and (ii) alters maternal allocation of reproductive resources to offspring quantity versus quality. 3. Results revealed that L. decemlineata mothers responded to perceived predation risk by producing clutches with fewer but larger eggs, thus increasing offspring provisioning. Surprisingly, while females that had faced predation risk as larva emerged with a similar body mass to control females, they exhibited lower metabolic rates. 4. Although predation risk in L. decemlineata larvae is known to impair their ability to acquire and maintain energy resources, adult females appeared to ameliorate such costs by improving their metabolic efficiency and by allocating more of their limited reproductive resources to produce fewer but better‐quality offspring.     

The starvation–predation risk trade-off, body mass and population status in the Common Starling Sturnus vulgaris

It is theoretically and empirically well established that body mass variation in small birds reflects a trade-off between starvation risk and predation risk. This occurs because carrying increased fat reserves reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, therefore, the theory of mass-dependent predation risk could be used to understand how a bird perceives and responds to the risks in its environment, because its mass will reflect the predictability of foraging opportunities and predation risk. Mass in birds may then provide a relatively straightforward way of assessing the foraging environment of birds and so the potential conservation problems a species faces. This study tests, for the first time for any species, how body mass changes in response to changing starvation risk, changing predation risk and changing population status. Common Starling Sturnus vulgaris mass varies as predicted by starvation–predation risk trade-off theory: mass is lower when foraging conditions are more favourable and when predation risk is increased. The populations that are declining the most strongly have higher mass, which is most likely indicative of a poor foraging environment, leading to lower relative survival. The results suggest that increased mass in Starlings, and possibly in other species, may provide an indication of the poor quality of the foraging environment and/or rapidly declining populations.     

Juvenile exposure to predator cues induces a larger egg size in fish

When females anticipate a hazardous environment for their offspring, they can increase offspring survival by producing larger young. Early environmental experience determines egg size in different animal taxa. We predicted that a higher perceived predation risk by juveniles would cause an increase in the sizes of eggs that they produce as adults. To test this, we exposed juveniles of the mouthbrooding cichlid Eretmodus cyanostictus in a split-brood experiment either to cues of a natural predator or to a control situation. After maturation, females that had been confronted with predators produced heavier eggs, whereas clutch size itself was not affected by the treatment. This effect cannot be explained by a differential female body size because the predator treatment did not influence growth trajectories. The observed increase of egg mass is likely to be adaptive, as heavier eggs gave rise to larger young and in fish, juvenile predation risk drops sharply with increasing body size. This study provides the first evidence that predator cues perceived by females early in life positively affect egg mass, suggesting that these cues allow her to predict the predation risk for her offspring.     

Optimal body size and energy expenditure during winter: why are voles smaller in declining populations?

Winter is energetically challenging for small herbivores because of greater energy requirements for thermogenesis at a time when little energy is available. We formulated a model predicting optimal wintering body size, accounting for the scaling of both energy expenditure and assimilation to body size, and the trade-off between survival benefits of a large size and avoiding survival costs of foraging. The model predicts that if the energy cost of maintaining a given body mass differs between environments, animals should be smaller in the more demanding environments, and there should be a negative correlation between body mass and daily energy expenditure (DEE) across environments. In contrast, if animals adjust their energy intake according to variation in survival costs of foraging, there should be a positive correlation between body mass and DEE. Decreasing temperature always increases equilibrium DEE, but optimal body mass may either increase or decrease in colder climates depending on the exact effects of temperature on mass-specific survival and energy demands. Measuring DEE with doubly labeled water on wintering Microtus agrestis at four field sites, we found that DEE was highest at the sites where voles were smallest despite a positive correlation between DEE and body mass within sites. This suggests that variation in wintering body mass between sites was due to variation in food quality/availability and not adjustments in foraging activity to varying risks of predation.     

Predation risk is unlikely to account for the failure of subordinate speckled warblers Chthonicola sagittata to help at the nest

The predator avoidance hypothesis suggests that the failure of subordinate birds to provision nestlings in communally breeding species is a consequence of increased predation risk. Parents exclude subordinates from the nest area and thus reduce the frequency of predator-attracting visits when the nest is most vulnerable, leading to increased reproductive success. I evaluated this hypothesis for the speckled warbler Chthonicola sagittata , a group-living member of the Pardalotidae in which subordinate males never feed nestlings or fledglings even though they are unrelated to the primary pair, compete for copulations and sometimes sire young in the brood. Parents did not modify provisioning behaviour relative to the risk of nest predation; provisioning rates to 10 d-old nestlings were similar on high and low risk territories. Furthermore, there was no evidence that parents modified the timing of deliveries or adjusted the relative size of deliveries in relation to predation risk. The condition (residual mass) of nestlings differed between high and low risk territories because nestlings on high risk territories had smaller tarsi but similar body mass to those at low risk. Tarsus length was the result of parental phenotype, not modified provisioning behaviour. Given that parents were unresponsive to predation risk, it seems unlikely that predation can account for the failure of subordinates to provision at the nest.     

Stabilizing selection on blue tit fledgling mass in the presence of sparrowhawks

Like British great tits, Belgian blue tits have a lower winter body mass when sparrowhawks are present. Since body mass affects manoeuvrability in small birds, tits may balance the risks of starvation and the risk of hawk predation by varying the amount of extra fat carried during winter. Predation pressure by sparrowhawks on young and inexperienced fledglings is at least as intense as that on the adults during winter. We therefore expected that tit fledgling body mass could also be reduced in the presence of sparrowhawks. In the years after one pair of sparrowhawks settled in a study plot, the mean body mass of blue tit fledglings was lower compared with that in years when there were no sparrowhawks. Furthermore, the shape of the curve relating juvenile survival to fledging mass changed, because the survival of the heaviest fledglings was reduced, which altered the selection differential of juvenile survival as a function of body mass from directional to stabilizing. Of seven published studies on the fledgling body mass–survival relation in tits, all three of the studies conducted in the absence of sparrowhawks showed the highest survival rates for the heaviest young, whereas in all four studies with sparrowhawks present this was no longer the case.     

Temporary flightlessness as a potential cost of reproduction in pre-laying Common Eiders Somateria mollissima

The rapid growth and reabsorption of the avian ovary is thought to be adaptive, as it reduces predation risk and the metabolic cost of flight. In this paper, we use an extreme case of parental investment to show how the survival of gravid birds may be impaired by reduced take-off ability. In still air, temporary flightlessness is regularly observed in female Common Eiders Somateria mollissima preparing for breeding. From a sample of pre-laying females collected in the Baltic Sea, we quantified the relationships among body reserves, organ mass and take-off ability using a general model of take-off performance. Average body mass at the beginning and end of follicular growth was, respectively, 32% and 43% higher than winter body mass. Wing-loading increased significantly during ovary development whereas the relative mass of flight muscles decreased. In contrast, organ mass and somatic body mass were constant from early follicular growth until laying, indicating that the observed increase in body mass was caused by ovary growth. The average specific lift production of individuals collected at the beginning of follicular growth was 9.7 N/kg, which is similar to the lift required to become airborne (9.8 N/kg). As ovary mass increased, lift production decreased to 9.2 N/kg at the onset of laying. These results indicate that temporary flightlessness results from the accumulation of large body reserves and subsequent ovarian growth. Predators of Common Eiders are diverse and may come from air, water and land. We suggest that temporary flightlessness may decrease adult survival through predation, and may represent an important cost of reproduction.     

Mass regulation in response to predation risk can indicate population declines

In theory, survival rates and consequent population status might be predictable from instantaneous behavioural measures of how animals prioritize foraging vs. avoiding predation. We show, for the 30 most common small bird species ringed in the UK, that one quarter respond to higher predation risk as if it is mass-dependent and lose mass. Half respond to predation risk as if it only interrupts their foraging and gain mass thus avoiding consequent increased starvation risk from reduced foraging time. These mass responses to higher predation risk are correlated with population and conservation status both within and between species (and independently of foraging habitat, foraging guild, sociality index and size) over the last 30 years in Britain, with mass loss being associated with declining populations and mass gain with increasing populations. If individuals show an interrupted foraging response to higher predation risk, they are likely to be experiencing a high quality foraging environment that should lead to higher survival. Whereas individuals that show a mass-dependent foraging response are likely to be in lower quality foraging environments, leading to relatively lower survival.     

The starvation-predation trade-off predicts trends in body size, muscularity, and adiposity between and within Taxa

The storage of lipids to buffer energy shortage may incur such costs as increased vulnerability to predation, and animals may be more muscular in order to reduce such costs. If muscle and lipid mass interact to determine survival, then both the muscularity and the adiposity of animals will be affected by factors such as predator density and food availability. Here we explore how adiposity and muscularity may depend on such factors. We confirm the expectation that adiposity should decrease with the risk of predation and increase with the frequency of interruptions to the food supply. More surprisingly, the predicted relationships between skeletal size, muscularity, and adiposity qualitatively depended on various factors: for example, adiposity should increase with foraging costs only for small animals and should decrease with total body mass if competition for food is intense. Furthermore, if the locomotive costs of carrying lipids are low, then adiposity should increase with body mass, whereas if such costs are high, then adiposity should decrease with body mass. These predictions are supported by observations of variation between and within species. Our approach demonstrates that broad patterns of body composition can be understood in terms of the fundamental ecological trade-off between starvation and predation.     

Survival to independence in relation to pre‐fledging development and latitude in songbirds across the globe

Species differ strongly in their life histories, including the probability of survival. Annual adult survival was investigated extensively in the past, whereas juvenile survival, and especially survival to independence, received much less attention. Yet, they are critical for our understanding of population demography and life‐history evolution. We investigated post‐fledging survival to independence (i.e. survival upon leaving the nest until nutritional independence) in 74 species of passerine birds worldwide based on 100 population level estimates extracted from published literature. Our comparative analyses revealed that survival to independence increased with the length of nestling period and relative fledging mass (ratio of fledging mass to adult body mass). At the same time, species with higher nest predation rates had shorter nestling periods and lower relative fledging mass. Thus, we identify an important trade‐off in life history strategies: staying longer in the nest may improve post‐fledging survival due to enhanced flight ability and sensory functions, but at the cost of a longer exposure to nest predators and increased mortality due to nest predation. Additionally, post‐fledging survival to independence did not differ between species from the northern temperate zone vs species from the tropics and southern hemisphere. However, analyses of post‐fledging survival curves suggest that 1) daily survival rates are not constant and improve quickly upon leaving the nest, and 2) species in the tropics and southern hemisphere have higher daily post‐fledging survival rates than northern temperate species. Nevertheless, due to the accumulation of mortality risk during their much longer periods of post‐fledging care, overall survival until independence is comparable across latitudes. Obtaining high‐quality demographic data across latitudes to evaluate the generality of these findings and mechanisms underlying them should be a research priority.     

Testing the mass-dependent predation hypothesis: in European blackbirds poor foragers have higher overwinter body reserves

As foraging becomes more unpredictable animals should increase their body reserves to reduce the risk of starvation. However, any increases in reserves may increase the risk of predation because extra mass probably compromises escape ability. Because of differences in foraging ability not all individuals will be affected in the same way by changes in foraging conditions. Relatively poor foragers will have more unpredictable foraging success for any given availability of food and therefore should carry larger body reserves. The mass-dependent predation hypothesis then predicts a negative correlation between levels of body reserves and foraging ability, although this may be modified by state-dependent compensation. I measured foraging rates and body masses of wintering European blackbirds, Turdus merula. Individuals with the lowest foraging rates had the largest gain in mass for the winter and had relatively high mass overall, independently of age and sex. That foraging rate determined mass rather than the reverse was demonstrated because foraging rate was independent of daily and seasonal mass change. Foraging rate within the experimental system was also independent of predation risk (as measured by distance from protective cover) and so the relation between mass and foraging rate was unlikely to have been confounded by any changes in vigilance to compensate for increased mass-dependent predation risk. The results suggest that blackbirds with high relative foraging rates have lower body reserves during the winter. Therefore there is probably a direct link between overwinter condition and fitness at least in blackbirds. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Causes and consequences of variation in offspring body mass: meta‐analyses in birds and mammals

Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta‐analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among‐study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass–survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (r_pearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass–offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.     

Evidence of the trade-off between starvation and predation risks in ducks

The theory of trade-off between starvation and predation risks predicts a decrease in body mass in order to improve flight performance when facing high predation risk. To date, this trade-off has mainly been validated in passerines, birds that store limited body reserves for short-term use. In the largest avian species in which the trade-off has been investigated (the mallard, Anas platyrhynchos), the slope of the relationship between mass and flight performance was steeper in proportion to lean body mass than in passerines. In order to verify whether the same case can be applied to other birds with large body reserves, we analyzed the response to this trade-off in two other duck species, the common teal (Anas crecca) and the tufted duck (Aythya fuligula). Predation risk was simulated by disturbing birds. Ducks within disturbed groups were compared to non-disturbed control birds. In disturbed groups, both species showed a much greater decrease in food intake and body mass during the period of simulated high risk than those observed in the control group. This loss of body mass allows reaching a more favourable wing loading and increases power for flight, hence enhancing flight performances and reducing predation risk. Moreover, body mass loss and power margin gain in both species were higher than in passerines, as observed in mallards. Our results suggest that the starvation-predation risk trade-off is one of the major life history traits underlying body mass adjustments, and these findings can be generalized to all birds facing predation. Additionally, the response magnitude seems to be influenced by the strategy of body reserve management.     

Impaired flight ability--a cost of reproduction in female blue tits

When prey are attacked by predators, escape ability has an obvious influence on the probability of survival. Laboratory studieshave suggested that flight performance of female birds mightbe affected by egg production. This is the first study of changesin take-off ability, and thus potentially in predation risk,during reproduction in wild birds. We trapped individual maleand female blue tits repeatedly during the breeding season.Females were 14% heavier and flew 20% slower (probably as aconsequence of a lower ratio of flight muscle to body mass)during the egg-laying period than after the eggs had hatched.However, flight muscle size did not change to compensate for changes in body mass over this period. In contrast, males showedno changes in either body mass, muscle size, or flight abilityover the same period. Furthermore, the impairment of flightin females increased with the proportion of the clutch thathad been laid, an effect that was independent of body mass and muscle size. This indicates that egg production causes additional physiological changes in the female body that produce impairedlocomotor performance. We suggest that courtship feeding offemale blue tits by their mates might reduce predation riskduring the period when female take-off ability is impairedby reducing the time females have to spend foraging and thusreducing the time they are exposed to increased predation.     

Winter compensatory growth under field conditions partly offsets low energy reserves before winter in a damselfly

Despite the survival value of high energy reserves during winter, animals often face energy deficits when entering winter. Compensatory growth in energy reserves during the winter period to buffer such deficits may increase winter survival and alleviate the need for costly compensatory mechanisms before or after winter when predation risk is much higher. However, such compensatory responses in energy reserves during winter have not been demonstrated under field conditions. We explored if Lestes eurinus damselfly larvae can compensate for suboptimal energy reserves during winter at 4°C when their ponds are covered with ice. In a field enclosure experiment, we demonstrated compensatory growth in terms of body mass and energy reserves in larvae whose energy status was previously manipulated in the laboratory. These results were supported by patterns in body mass and energy reserves over winter in two natural unmanipulated populations. Winter survival was high overall and not affected by compensatory growth. We hypothesize that the observed compensatory growth in energy reserves during winter may shape life history decisions in autumn and spring, and may make resource availability during winter as or more important than energy reserves before winter.     

Density-dependent nest predation in waterfowl: the relative importance of nest density versus nest dispersion

When nest predation levels are very high or very low, the absolute range of observable nest success is constrained (a floor/ceiling effect), and it may be more difficult to detect density-dependent nest predation. Density-dependent nest predation may be more detectable in years with moderate predation rates, simply because there can be a greater absolute difference in nest success between sites. To test this, we replicated a predation experiment 10 years after the original study, using both natural and artificial nests, comparing a year when overall rates of nest predation were high (2000) to a year with moderate nest predation (2010). We found no evidence for density-dependent predation on artificial nests in either year, indicating that nest predation is not density-dependent at the spatial scale of our experimental replicates (1-ha patches). Using nearest-neighbor distances as a measure of nest dispersion, we also found little evidence for "dispersion-dependent" predation on artificial nests. However, when we tested for dispersion-dependent predation using natural nests, we found that nest survival increased with shorter nearest-neighbor distances, and that neighboring nests were more likely to share the same nest fate than non-adjacent nests. Thus, at small spatial scales, density-dependence appears to operate in the opposite direction as predicted: closer nearest neighbors are more likely to be successful. We suggest that local nest dispersion, rather than larger-scale measures of nest density per se, may play a more important role in density-dependent nest predation.     

Overwinter mass loss of snowshoe hares in the Yukon: starvation, stress, adaptation or artefact?

1. Overwinter mass loss can reduce energetic requirements in mammals (Dehnel's phenomenon). Alternatively, mass loss can result from food limitation or high predation risk. 2. We use data from fertilizer, food-supplementation and predator-exclusion experiments in the Yukon during a population cycle from 1986 to 1996 to test the causes of overwinter mass loss by snowshoe hares (Lepus americanus). In all years, some hares on control sites gained mass overwinter. During the increase phase the majority gained mass, but in all other phases the majority lost mass. 3. Snowshoe hares weighing <1000 g in autumn always gained mass overwinter, as did the majority that weighed 1000-1400 g. Hares weighing >1800 g in autumn usually lost mass. 4. Snowshoe hares on the predator-exclosure + food site gained mass overwinter in all years. Hares on the food-supplementation sites lost mass during the decline but gained mass in all other phases. Fertilization had little effect on mass dynamics. 5. Snowshoe hares were more likely to lose mass during winters with low survival rates. Snowshoe hares on the predator-exclosure treatments were more likely to gain mass than were hares on control sites. 6. Overwinter mass loss was correlated with maximum snow depth. At equivalent snow depths, hares on food-supplemented areas lost 98 g (+/- 14.6 SE) less on average than hares on the controls and predator-exclosure treatment. 7. Bone-marrow fat was related to body mass and cause of death. Small hares had the lowest marrow fat. Hares killed by humans had higher marrow fat than those killed by predators; hares that simply died had the lowest marrow fat. Hares on food-supplemented sites had the highest kidney and marrow fat. 8. Overwinter-mass loss for snowshoe hares is explained interactively by winter conditions, food supply, predation risk and autumn mass. Some snowshoe hares lost mass overwinter in all years and on all treatments, suggesting that reducing body mass may facilitate survival, especially in cases where foraging costs are high energetically or increase predation risk.