The costs of being cool: a dynamic model of nocturnal hypothermia by small food-caching birds in winter

Many birds could expend substantially less energy at night by using hypothermia, but generally do not. This suggests that the potential savings are offset by costs; one of these costs is presumed to be the risk of predation at night. If this assumption is correct, a bird will face one of two tradeoffs: (1) it can avoid the cost of hypothermia by gaining fat to decrease the risk of starvation, but this increases energetic costs of fat maintenance and risk of diurnal predation, or (2) it can maintain lower fat reserves and use hypothermia at night, but this option increases the risk of nocturnal predation. We used a dynamic model to investigate these trade-offs and how the use of nocturnal hypothermia changes energy management tactics in food-caching birds. Our model predicted that: (i) optimal daily routines of fat reserves, feeding rate, food caching, and cache retrieval should be similar in hypothermic and non-hypothermic birds; (ii) low fat reserves, small cache size, low ambient temperature, and high variability in foraging success favor increased use of hypothermia; (iii) the effect of ambient temperature on the use of hypothermia is especially important at higher levels of variance in foraging success; (iv) hypothermic birds are predicted to have lower mass at dusk than non-hypothermic individuals while their morning mass should be more similar. Many of these predictions have been supported by empirical data. Also, survival rates are predicted to be higher for birds using hypothermia, especially in the most severe environmental conditions. This is the first attempt to evaluate the role of cache maintenance and variance in foraging success in the use of hypothermia. This is also the first discussion of the relationship between behavior hypothermia and diurnal patterns of energy management.     

Avian daily foraging patterns: Effects of digestive constraints and variability

Summary Birds show a typical daily pattern of heavy morning and secondary afternoon feeding. We investigate the pattern of foraging by a bird that results in the lowest long-term rate of mortality. We assume the following: mortality is the sum of starvation and predation. The bird is characterized by two state variables, its energy reserves and the amount of food in its stomach. Starvation occurs during the day if the bird's reserves fall to zero. The bird starves during the night if the total energy stored in reserves and the stomach is less than a critical amount. The probability that the bird is killed by a predator is higher if the bird is foraging than if it is resting. Furthermore, the predation risk while foraging increases with the bird's mass. From these assumptions, we use dynamic programming techniques to find the daily foraging routine that minimizes mortality. The principal results are (1) Variability in food finding leads to routines with feeding concentrated early in the day, (2) digestive constraints cause feeding to be spread more evenly through the day, (3) even under fairly severe digestive constraints, the stomach is generally not full and (4) optimal fat reserve levels are higher in more variable environments and under digestive constraints. This model suggests that the characteristic daily feeding pattern of small birds is not due to digestive constraints but is greatly influenced by environmental variability.     

Exploring the role of vision in social foraging: What happens to group size,vigilance, spacing,aggression and habitat use in birds and mammals that forage at night?

I examined the role of vision in social foraging by contrasting group size, vigilance, spacing, aggression and habitat use between day and night in many species of birds and mammals. The literature review revealed that the rate of predation/disturbance was often reduced at night while food was considered more available. Social foraging at night was prevalent in many species suggesting that low light levels at night are not sufficient to prevent the formation and cohesion of animal groups. Group sizes were similar or larger at night than during the day in more than half the bird populations and in the majority of mammal populations. Factors such as calls, feeding noises or smells may contribute to the formation and cohesion of groups at night. Larger numbers of foragers at night may also facilitate the aggregation of more foragers. Vigilance levels were usually lower at night perhaps as a response to the lower predation risk or to the decreased value of scanning for predators that are difficult to locate. Low light levels may also make visual cues that promote aggression less conspicuous, which may be a factor in the lower levels of aggression documented at night. Spacing varied as a function of time of day in response to changes in foraging mode or food availability. Habitats that are avoided during the day were often used at night. Foraging at night presents birds and mammals with a new set of constraints that influence group size, time budgeting and habitat use.     

Optimal diving under the risk of predation

Many air-breathing aquatic foragers may be killed by aerial or subsurface predators while recovering oxygen at the surface; yet the influence of predation risk on time allocation during dive cycles is little known in spite of numerous studies on optimal diving. We modeled diving behavior under the risk of predation at the surface. The relationship between time spent at the surface and the risk of death is predicted to influence the optimal surface interval, regardless of whether foragers accumulate energy at a constant rate while at the food patch, deplete food resources over the course of the dive, or must search for food during the dive. When instantaneous predation risk during a single surface interval decreases with time spent at the surface, a diver should increase its surface interval relative to that which maximizes energy intake, thereby increasing dive durations and reducing the number of surfacings per foraging bout. When instantaneous risk over a single surface interval does not change or increases with increasing time at the surface, divers should decrease their surface interval (and consequently their dive duration) relative to that which maximizes energy intake resulting in more dives per foraging bout. The fitness consequences of selecting a suboptimal surface interval vary with the risk function and the way divers harvest energy when at depth. Finally, predation risk during surface intervals should have important consequences for habitat selection and other aspects of the behavioral ecology of air-breathing aquatic organisms.     

Dynamics of herbivores and resources on a landscape with interspersed resources and refuges

A tradeoff between energy gain from foraging and safety from predation in refuges is a common situation for many herbivores that are vulnerable to predation while foraging. This tradeoff affects the population dynamics of the plant–herbivore–predator interaction. A new functional response is derived based on the Holling type 2 functional response and the assumption that the herbivore can forage at a rate that maximizes its fitness. The predation rate on the herbivore is assumed to be proportional to the product of the time that the herbivore spends foraging and a risk factor that reflects the habitat complexity; where greater complexity means greater interspersion of high food quality habitat and refuge habitat, which increases the amount of the edge zone between refuge and foraging areas, making foraging safer. The snowshoe hare is chosen as an example to demonstrate the resulting dynamics of an herbivore that has been intensely studied and that undergoes well-known cycling. Two models are studied in which the optimal foraging by hares is assumed, a vegetation–hare–generalist predator model and a vegetation–hare–specialist predator model. In both cases, the results suggest that the cycling of the snowshoe hare population will be greatly moderated by optimal foraging in a habitat consisting of interspersed high quality foraging habitat and refuge habitat. However, there are also large differences in the dynamics produced by the two models as a function of predation pressure.     

Indirect risk effects reduce feeding efficiency of ducks during spring

Indirect risk effects of predators on prey behavior can have more of an impact on prey populations than direct consumptive effects. Predation risk can elicit more vigilance behavior in prey, reducing the amount of time available for other activities, such as foraging, which could potentially reduce foraging efficiency. Understanding the conditions associated with predation risk and the specific effects predation risk have on prey behavior is important because it has direct influences on the profitability of food items found under various conditions and states of the forager. The goals of this study were to assess how ducks perceived predation risk in various habitat types and how strongly perceived risk versus energetic demand affected foraging behavior. We manipulated food abundance in different wetland types in Illinois, USA to reduce confounding between food abundance and vegetation structure. We conducted focal‐animal behavioral samples on five duck species in treatment and control plots and used generalized linear mixed‐effects models to compare the effects of vegetation structure versus other factors on the intensity with which ducks fed and the duration of feeding stints. Mallards fed more intensively and, along with blue‐winged teal, used longer feeding stints in open habitats, consistent with the hypothesis that limited visibility was perceived to have a greater predation risk than unlimited visibility. The species temporally nearest to nesting, wood ducks, were willing to take more risks for a greater food reward, consistent with an increase in a marginal value of energy as they approached nesting. Our results indicate that some duck species value energy differently based on the surrounding vegetation structure and density. Furthermore, increases in the marginal value of energy can be more influential than perceived risk in shaping foraging behavior patterns. Based on these findings, we conclude that the value of various food items is not solely determined by energy contained in the item but by conditions in which it is found and the state of the forager.     

Foraging behavior in stochastic environments

How do temporally stochastic environments affect risk sensitivity in foraging behavior? We build a simple model of foraging under predation risks in stochastic environments, where the environments change over generations. We analyze the effects of stochastic environments on risk sensitivity of foraging animals by means of the difference between the geometric mean fitness and the arithmetic mean fitness. We assume that foraging is associated with predation risks whereas resting in the nest is safe because it is free of predators. In each generation, two different environments with given food amounts and predation risks occur with a certain probability. The geometric mean optimum is independent of food amounts. In most cases of stochastic environments, risk-averse tendency is increased, but in some limited conditions, more risk-prone behavior is favored. Specifically, risk-prone tendency is increased when the variation in food amount increases. Our results imply that the optimal behavior depends on the probability distribution of environmental effects under all selection regimes.     

Predation risk influences food‐web structure by constraining species diet choice

The foraging behaviour of species determines their diet and, therefore, also emergent food‐web structure. Optimal foraging theory (OFT) has previously been applied to understand the emergence of food‐web structure through a consumer‐centric consideration of diet choice. However, the resource‐centric viewpoint, where species adjust their behaviour to reduce the risk of predation, has not been considered. We develop a mechanistic model that merges metabolic theory with OFT to incorporate the effect of predation risk on diet choice to assemble food webs. This ‘predation‐risk‐compromise’ (PR) model better captures the nestedness and modularity of empirical food webs relative to the classical optimal foraging model. Specifically, compared with optimal foraging alone, risk‐mitigated foraging leads to more‐nested but less‐modular webs by broadening the diet of consumers at intermediate trophic levels. Thus, predation risk significantly affects food‐web structure by constraining species’ ability to forage optimally, and needs to be considered in future work.     

Effects of predatory risk and resource renewal on the timing of foraging activity in a gerbil community

The foraging decisions of animals are often influenced by risk of predation and by the renewal of resources. For example, seed-eating gerbils on sand dunes in the Negev Desert of Israel prefer to forage in the bush microhabitat and during darker hours due to risk of predation. Also, daily renewal of seed resource patches and timing of nightly foraging activity in a depleting environment play important roles in species coexistence. We examined how these factors influence the timing of gerbil foraging by quantifying foraging activity in seed resource patches that we experimentally renewed hourly during the night. As in previous work, gerbils showed strong preference for the safe bush microhabitat and foraged less in response to high levels of illumination from natural moon light and from artificial sources. We demonstrate here for the first time that gerbils also responded to temporal and spatial heterogeneity in predatory risk through their timing of activity over the course of each night. Typically, gerbils concentrated their activity early in the night, but this changed with moon phase and in response to added illumination. These results can be understood in terms of the nature of patch exploitation by gerbils and the role played by the marginal value of energy in determining the cost of predation. They further show the dynamic nature of gerbil foraging decisions, with animals altering foraging efforts in response to time, microhabital, moon phase, illumination, and resource availability.     

Diurnal foraging routines in a tropical bird,the rock finch Lagonosticta sanguinodorsalis: how important is predation risk?

An animal's foraging decisions are the outcome of the relative importance of the risk of starvation and predation. Fat deposition insures against periods of food shortage but it also carries a cost in terms of mass dependent predation risk due to reduced escape probability and extended exposure time. Accordingly, birds have been observed to show a unimodal foraging pattern with foraging concentrated at the end of the day under conditions of predictable food resources and high predation risk. We tested this hypothesis in a tropical granivorous finch, the rock firefinch Lagonosticta sanguinodorsalis , in an outdoor aviary experiment during which food was provided ad lib and the risk of predation was varied by providing food either adjacent to, or 5 m away from cover. Rock firefinches showed a bimodal foraging pattern regardless of the risk of predation at which they fed. The results suggest that predation is relatively unimportant in shaping their daily feeding pattern despite mass gain during the day being similar to temperate birds. Foraging patterns closely follow diurnal temperature variation and this is suggested to be the main determinant of the observed bimodal pattern.     

Fatness and fitness: exposing the logic of evolutionary explanations for obesity

To explore the logic of evolutionary explanations of obesity we modelled food consumption in an animal that minimizes mortality (starvation plus predation) by switching between activities that differ in energy gain and predation. We show that if switching does not incur extra predation risk, the animal should have a single threshold level of reserves above which it performs the safe activity and below which it performs the dangerous activity. The value of the threshold is determined by the environmental conditions, implying that animals should have variable ‘set points’. Selection pressure to prevent energy stores exceeding the optimal level is usually weak, suggesting that immediate rewards might easily overcome the controls against becoming overweight. The risk of starvation can have a strong influence on the strategy even when starvation is extremely uncommon, so the incidence of mortality during famine in human history may be unimportant for explanations for obesity. If there is an extra risk of switching between activities, the animal should have two distinct thresholds: one to initiate weight gain and one to initiate weight loss. Contrary to the dual intervention point model, these thresholds will be inter-dependent, such that altering the predation risk alters the location of both thresholds; a result that undermines the evolutionary basis of the drifty genes hypothesis. Our work implies that understanding the causes of obesity can benefit from a better understanding of how evolution shapes the mechanisms that control body weight.     

Using habitat selection theories to predict the spatiotemporal distribution of migratory birds during stopover – a case study of pink‐footed geese Anser brachyrhynchus

Understanding how animals select for habitat and foraging resources therein is a crucial component of basic and applied ecology. The selection process is typically influenced by a variety of environmental conditions including the spatial and temporal variation in the quantity and quality of food resources, predation or disturbance risks, and inter‐ and intraspecific competition. Indeed, some of the most commonly employed ecological theories used to describe how animals choose foraging sites are: nutrient intake maximisation, density‐dependent habitat selection, central‐place foraging, and predation risk effects. Even though these theories are not mutually exclusive, rarely are multiple theoretical models considered concomitantly to assess which theory, or combination thereof, best predicts observed changes in habitat selection over space and time. Here, we tested which of the above theories best‐predicted habitat selection of Svalbard‐breeding pink‐footed geese at their main spring migration stopover site in mid‐Norway by computing a series of resource selection functions (RSFs) and their predictive ability (k‐fold cross validation scores). At this stopover site geese fuel intensively as a preparation for breeding and further migration. We found that the predation risk model and a combination of the density‐dependent and central‐place foraging models best‐predicted habitat selection during stopover as geese selected for larger fields where predation risk is typically lower and selection for foraging sites changed as a function of both distance to the roost site (i.e. central‐place) and changes in local density. In contrast to many other studies, the nutritional value of the available food resources did not appear to be a major limiting factor as geese used different food resources proportional to their availability. Our study shows that in an agricultural landscape where nutritional value of food resources is homogeneously high and resource availability changes rapidly; foraging behaviour of geese is largely a tradeoff between fast refuelling and disturbance/predator avoidance.     

Maximising survival by shifting the daily timing of activity

Maximising survival requires animals to balance the competing demands of maintaining energy balance and avoiding predation. Here, quantitative modelling shows that optimising the daily timing of activity and rest based on the encountered environmental conditions enables small mammals to maximise survival. Our model shows that nocturnality is typically beneficial when predation risk is higher during the day than during the night, but this is reversed by the energetic benefit of diurnality when food becomes scarce. Empirical testing under semi‐natural conditions revealed that the daily timing of activity and rest in mice exposed to manipulations in energy availability and perceived predation risk is in line with the model’s predictions. Low food availability and decreased perceived daytime predation risk promote diurnal activity patterns. Overall, our results identify temporal niche switching in small mammals as a strategy to maximise survival in response to environmental changes in food availability and perceived predation risk.     

Hazardous duty pay and the foraging cost of predation

We review the concepts and research associated with measuring fear and its consequences for foraging. When foraging, animals should and do demand hazardous duty pay. They assess a foraging cost of predation to compensate for the risk of predation or the risk of catastrophic injury. Similarly, in weighing foraging options, animals tradeoff food and safety. The foraging cost of predation can be modelled, and it can be quantitatively and qualitatively measured using risk titrations. Giving‐up densities (GUDs) in depletable food patches and the distribution of foragers across safe and risky feeding opportunities are two frequent experimental tools for titrating food and safety. A growing body of literature shows that: (i) the cost of predation can be big and comprise the forager's largest foraging cost, (ii) seemingly small changes in habitat or microhabitat characteristics can lead to large changes in the cost of predation, and (iii) a forager's cost of predation rises with risk of mortality, the forager's energy state and a decrease in its marginal value of energy. In titrating for the cost of predation, researchers have investigated spatial and temporal variation in risk, scale‐dependent variation in risk, and the role of predation risk in a forager's ecology. A risk titration from a feeding animal often provides a more accurate behavioural indicator of predation risk than direct observations of predator‐inflicted mortality. Titrating for fear responses in foragers has some well‐established applications and holds promise for novel methodologies, concepts and applications. Future directions for expanding conceptual and empirical tools include: what are the consequences of foraging costs arising from interference behaviours and other sources of catastrophic loss? Are there alternative routes by which organisms can respond to tradeoffs of food and safety? What does an animal's landscape of fear look like as a spatially explicit map, and how do various environmental factors affect it? Behavioural titrations will help to illuminate these issues and more.     

An energy-based model of optimal feeding-territory size

An energy-based model of feeding territoriality is described. The model predicts an optimal territory size where the territory holder's net energy intake is maximized, on a daily or seasonal time scale. Simulated effects on optimal territory size of animal size, food availability, and competitor density are in general agreement with observed relationships in a wide variety of animals. When salmonid data are used to estimate the model parameter values, predicted territory sizes are similar to those actually observed. When emigration is allowed, the model predicts that territoriality, through individual selection alone, can regulate population size, but that this regulation breaks down when initial densities exceed some threshold value. Sensitivity analysis shows optimal territory size to be most affected by those parameters influencing food intake and energy expenditure. Some alternative criteria for optimization are also discussed. An animal maximizing net foraging efficiency has a smaller territory than one maximizing net energy, but the effects of animal size, food availability, and competitor density on territory size are the same in either case.     

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.     

Temporal changes in food preferences of wood mice (Apodemus sylvaticus L.)

Diet choice was determined for wild-caught wood mice (Apodemus sylvaticus L.), temporarily confined to cages in the field and offered a choice of 24–26 types of seeds and fruits in 2-h sessions throughout the night. The mice showed an overall preference for some foods over others. The set-up minimized influences on food preferences of predation risk, hunger, food availability and competition. Variation in food preferences was not attributable to differences between individuals, but followed a temporal pattern. The variety of foods eaten showed a bimodal pattern with peaks corresponding to the two most active periods at the beginning and end of the night. Both the amount of food eaten and variation in the amount diminished from the first to the second active period. An expected selection for carbohydrates early in the night and proteins at the end of the night was not found, but sugars were selected for early in the night. These results are discussed in relation to the conflict between an animal's continuous energy requirements and the essentially periodic activity of foraging.     

A dynamic habitat selection game

A patch selection game is formulated and analyzed. Organisms can forage in one of H patches. Each patch is characterized by the cost of foraging, the density and value of food, the predation risk, and the density of conspecifics. The presence of conspecifics affects the finding and sharing of food, and the predation risk. Optimal foraging theory can be viewed as a "1-person" game against nature in which the optimal patch choice of a specific organism is analyzed assuming that the number of conspecifics in other patches is fixed. In the general game theoretic approach, the behavior of conspecifics is included in the determination of the distinguished organism's strategy. An iterative algorithm is used to compute the solution of the "n-person" game or dynamic ESS, which differs from the optimal foraging theory solution. Experiments to test the proposed theory using rodents and seed trays are briefly discussed.     

Prey susceptibilities,prey utilization and variable attack efficiencies of Ural owls

Summary To investigate the factors that influence prey utilization among predators with active prey, three series of experiments were performed in which Ural owls (Strix uralensis) searched for and attacked three prey species of wild mice, Microtus montebelli, Apodemus speciosus, and A. argenteus, in a large flight cage. Over the whole study, owls attacked mice about ten times a night. The number of attacks on each prey species did not differ from that predicted by a random attack model. M. montebelli was taken more than either Apodemus species. Prey utilization appears to be influenced by prey susceptibilities only and it is unlikely that prey selection by the owls affected prey utilization patterns. Under the experimental conditions, random attack is predicted by optimal foraging theory. However, random attack may be explained just as well by the inability of the owl to discriminate prey type. The owls, energy gain was adjusted not by alteration in the number of attacks on a prey species but rather by alteration in the capture success between experiments. Capture success increased in poor food conditions for the same prey species. This flexibility in capture success has not been considered in the assumptions of optimal foraging theory. In conventional optimal foraging theory, the probability of capture success is implicitly assumed as constant and unity. We suggest that this assumption is inadequate to understand the foraging behavior of owls.     

Patch use in time and space for a meso-predator in a risky world

Predator–prey studies often assume a three trophic level system where predators forage free from any risk of predation. Since meso-predators themselves are also prospective prey, they too need to trade-off between food and safety. We applied foraging theory to study patch use and habitat selection by a meso-predator, the red fox. We present evidence that foxes use a quitting harvest rate rule when deciding whether or not to abandon a foraging patch, and experience diminishing returns when foraging from a depletable food patch. Furthermore, our data suggest that patch use decisions of red foxes are influenced not just by the availability of food, but also by their perceived risk of predation. Fox behavior was affected by moonlight, with foxes depleting food resources more thoroughly (lower giving-up density) on darker nights compared to moonlit nights. Foxes reduced risk from hyenas by being more active where and when hyena activity was low. While hyenas were least active during moon, and most active during full moon nights, the reverse was true for foxes. Foxes showed twice as much activity during new moon compared to full moon nights, suggesting different costs of predation. Interestingly, resources in patches with cues of another predator (scat of wolf) were depleted to significantly lower levels compared to patches without. Our results emphasize the need for considering risk of predation for intermediate predators, and also shows how patch use theory and experimental food patches can be used for a predator. Taken together, these results may help us better understand trophic interactions.