Foraging patterns of voles at heterogeneous avian and uniform mustelid predation risk

Temporal variation of antipredatory behavior and a uniform distribution of predation risk over refuges and foraging sites may create foraging patterns different from those anticipated from risk in heterogenous habitats. We studied the temporal variation in foraging behavior of voles exposed to uniform mustelid predation risk and heterogeneous avian predation risk of different levels induced by vegetation types in eight outdoor enclosures (0.25 ha). We manipulated mustelid predation risk with weasel presence or absence and avian predation risk by reducing or providing local cover at experimental food patches. Foraging at food patches was monitored by collecting giving-up densities at artificial food patches, overall activity was automatically monitored, and mortality of voles was monitored by live-trapping and radiotracking. Voles depleted the food to lower levels in the sheltered patches than in the exposed ones. In enclosures with higher avian predation risk caused by lower vegetation height, trays were depleted to lower levels. Unexpectedly, voles foraged in more trays and depleted trays to lower levels in the presence of weasels than in the absence. Weasels match their prey's body size and locomotive abilities and therefore increase predation risk uniformly over both foraging sites and refuge sites that can both be entered by the predator. This reduces the costs of missing opportunities other than foraging. Voles changed their foraging strategy accordingly by specializing on the experimental food patches with predictable returns and probably reduced their foraging in the matrix of natural food source with unpredictable returns and high risk to encounter the weasel. Moreover, after 1 day of weasel presence, voles shifted their main foraging activities to avoid the diurnal weasel. This behavior facilitated bird predation, probably by nocturnal owls, and more voles were killed by birds than by weasels. Food patch use of voles in weasel enclosures increased with time. Voles had to balance the previously missed feeding opportunities by progressively concentrating on artificial food patches.     

Ecological Risk Aversion and Foraging Behaviors of Juvenile Squirrel Monkeys (Saimiri sciureus)

The ‘ecological risk aversion hypothesis’ [C.H. Janson and C.P. van Schaik, Juvenile Primates, Oxford Univ. Press, New York (1993), pp. 57–74] proposes that the pattern of slow growth characteristic of juvenile primates is a response to ecological risks (predation and starvation) experienced by juveniles. Juveniles are thought to avoid predation risk by positioning themselves near conspecifics, therefore experiencing high levels of feeding competition with older individuals, reduced access to resources and, consequently, high starvation risks during periods of food scarcity. The present study compared the foraging behaviors of juvenile and adult squirrel monkeys, a small neotropical primate characterized by a long juvenile period, to determine how predation and starvation risks affected juvenile behaviors. The study was conducted in Eastern Amazonia, in a seasonal environment. Due to their slow development, small body size and large group sizes, it was expected that juveniles in this species would behave in a manner consistent with the risk aversion hypothesis. However, age differences in foraging efficiency and foraging success were smaller than predicted. There was also no evidence that juveniles sacrificed access to food for predator protection. Adults did not have preferential access to fruit patches and direct competition was rare. Feeding competition for prey, the most common resource in the troop's diet, was negligible. Therefore, the slow growth and long juvenile period of squirrel monkeys do not correspond with evidence of predation or starvation risk, as predicted by the risk aversion hypothesis.     

Evaluation of predation risk in the collectively foraging termite Macrotermes bellicosus

Summary. Few studies have investigated foraging decisions in collectively foraging social insects with no studies in termites. In termites predation is assumed to be a key mortality factor. Therefore, we experimentally investigated the role of predation pressure in foraging decisions of the fungus cultivating, mound building termite Macrotermes bellicosus in two habitats of the Comoé National Park (Ivory Coast). We used the indirect approach of measuring the Giving up Density (GUD), which is the amount of food left when individuals stop foraging in a food patch, whilst experimentally varying predation pressure. Three different conditions were examined: (a) natural predation, (b) no predation, and (c) experimental predation through artificial removal of termites. In the shrub savanna, foraging termites responded to increasing predation with increasing GUDs. By contrast, in the gallery forest, there was no gradual response. Instead termites abandoned a food patch immediately after an attack by predators. Without predation GUDs were lower in the savanna than in the gallery forest indicating that food had a higher value in the former habitat. This, together with the differential behavioral responses to predation, was in accordance with high availability of food in the gallery forest and a limited supply of food in the savanna. Thus, according to our results termites traded off predation pressure differently, according to the availability of food in both habitats.     

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.     

Samango Monkeys (<Emphasis Type="Italic">Cercopithecus albogularis labiatus</Emphasis>) Manage Risk in a Highly Seasonal,Human-Modified Landscape in Amathole Mountains,South Africa

Wild species use habitats that vary in risk across space and time. This risk can derive from natural predators and also from direct and indirect human pressures. A starving forager will often take risks that a less hungry forager would not. At a highly seasonal and human-modified site, we predicted that arboreal samango monkeys (Cercopithecus albogularis labiatus) would show highly flexible, responsive, risk-sensitive foraging. We first determined how monkeys use horizontal and vertical space across seasons to evaluate if high-risk decisions (use of gardens and ground) changed with season, a proxy for starvation risk. Then, during a subsequent winter, we offered equal feeding opportunities (in the form of high-value, raw peanuts) in both gardens and forest to see if this short-term change in food availability and starvation risk affected monkeys’ foraging decisions. We found that during the food-scarce winter, monkeys foraged outside indigenous forest and in gardens, where they fed on exotic species, especially fallen acorns (Quercus spp.), despite potential threats from humans. Nevertheless, and as predicted, when given the choice of foraging on high-value foods in gardens vs. forest during our artificial foraging experiment, monkeys showed a preference for a safer forest habitat. Our experiment also indicated monkeys’ sensitivity to risk in the lower vertical strata of both habitats, despite their previous extensive use of the ground. Our findings support one of the central tenets of optimal foraging theory: that risk of starvation and sensitivity to the variation in food availability can be as important drivers of behavior as risk of predation.     

The dilemma of foraging herbivores: dealing with food and fear

For foraging herbivores, both food quality and predation risk vary across the landscape. Animals should avoid low-quality food patches in favour of high-quality ones, and seek safe patches while avoiding risky ones. Herbivores often face the foraging dilemma, however, of choosing between high-quality food in risky places or low-quality food in safe places. Here, we explore how and why the interaction between food quality and predation risk affects foraging decisions of mammalian herbivores, focusing on browsers confronting plant toxins in a landscape of fear. We draw together themes of plant–herbivore and predator–prey interactions, and the roles of animal ecophysiology, behaviour and personality. The response of herbivores to the dual costs of food and fear depends on the interplay of physiology and behaviour. We discuss detoxification physiology in dealing with plant toxins, and stress physiology associated with perceived predation risk. We argue that behaviour is the interface enabling herbivores to stay or quit food patches in response to their physiological tolerance to these risks. We hypothesise that generalist and specialist herbivores perceive the relative costs of plant defence and predation risk differently and intra-specifically, individuals with different personalities and physiologies should do so too, creating individualised landscapes of food and fear. We explore the ecological significance and emergent impacts of these individual-based foraging outcomes on populations and communities, and offer predictions that can be clearly tested. In doing so, we provide an integrated platform advancing herbivore foraging theory with food quality and predation risk at its core.     

Ecological correlates of interindividual distance in the St. Kitts veret (Cercopithecus aethiops sabaeus)

Field data were collected on a free ranging population of vervet monkeys (Cercopithecus aethiops sabaeus) on St. Kitts to test four hypotheses relating cover, risk of predation, and food density to interindividual distance. The results indicated that when food was not a factor, interindividual distance was positively related to the amount of cover in the immediate environment, and therefore to risk of predation. When cover was held constant, distance was inversely related to food density. When the minimum distance for optimal foraging was greater than that required for safety, a compromise distance intermediate between the two predicted values was observed. Cover and food density also predicted the inverse relationship found between age-sex class and interindividual distance. Implications of the above in relation to interindividual competition are discussed.     

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 Perception,Food Density and Conspecific Cues Shape Foraging Decisions in a Tropical Lizard

When foraging, animals can maximize their fitness if they are able to tailor their foraging decisions to current environmental conditions. When making foraging decisions, individuals need to assess the benefits of foraging while accounting for the potential risks of being captured by a predator. However, whether and how different factors interact to shape these decisions is not yet well understood, especially in individual foragers. Here we present a standardized set of manipulative field experiments in the form of foraging assays in the tropical lizard Anolis cristatellus in Puerto Rico. We presented male lizards with foraging opportunities to test how the presence of conspecifics, predation-risk perception, the abundance of food, and interactions among these factors determines the outcome of foraging decisions. In Experiment 1, anoles foraged faster when food was scarce and other conspecifics were present near the feeding tray, while they took longer to feed when food was abundant and when no conspecifics were present. These results suggest that foraging decisions in anoles are the result of a complex process in which individuals assess predation risk by using information from conspecific individuals while taking into account food abundance. In Experiment 2, a simulated increase in predation risk (i.e., distance to the feeding tray) confirmed the relevance of risk perception by showing that the use of available perches is strongly correlated with the latency to feed. We found Puerto Rican crested anoles integrate instantaneous ecological information about food abundance, conspecific activity and predation risk, and adjust their foraging behavior accordingly.     

Great tits search for,capture, kill and eat hibernating bats

Ecological pressure paired with opportunism can lead to surprising innovations in animal behaviour. Here, we report predation of great tits (Parus major) on hibernating pipistrelle bats (Pipistrellus pipistrellus) at a Hungarian cave. Over two winters, we directly observed 18 predation events. The tits specifically and systematically searched for and killed bats for food. A substantial decrease in predation on bats after experimental provisioning of food to the tits further supports the hypothesis that bat-killing serves a foraging purpose in times of food scarcity. We finally conducted a playback experiment to test whether tits would eavesdrop on calls of awakening bats to find them in rock crevices. The tits could clearly hear the calls and were attracted to the loudspeaker. Records for tit predation on bats at this cave now span more than ten years and thus raise the question of whether cultural transmission plays a role for the spread of this foraging innovation.     

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.     

Plant Defenses and Predation Risk Differentially Shape Patterns of Consumption,Growth, and Digestive Efficiency in a Guild of Leaf-Chewing Insects

Herbivores are squeezed between the two omnipresent threats of variable food quality and natural enemy attack, but these two factors are not independent of one another. The mechanisms by which organisms navigate the dual challenges of foraging while avoiding predation are poorly understood. We tested the effects of plant defense and predation risk on herbivory in an assemblage of leaf-chewing insects on Solanum lycopersicum (tomato) that included two Solanaceae specialists (Manduca sexta and Leptinotarsa decemlineata) and one generalist (Trichoplusia ni). Defenses were altered using genetic manipulations of the jasmonate phytohormonal cascade, whereas predation risk was assessed by exposing herbivores to cues from the predaceous stink bug, Podisus maculiventris. Predation risk reduced herbivore food intake by an average of 29% relative to predator-free controls. Interestingly, this predator-mediated impact on foraging behavior largely attenuated when quantified in terms of individual growth rate. Only one of the three species experienced lower body weight under predation risk and the magnitude of this effect was small (17% reduction) compared with effects on foraging behavior. Manduca sexta larvae, compensated for their predator-induced reduction in food intake by more effectively converting leaf tissue to body mass. They also had higher whole-body lipid content when exposed to predators, suggesting that individuals convert energy to storage forms to draw upon when risk subsides. In accordance with expectations based on insect diet breadth, plant defenses tended to have a stronger impact on consumption and growth in the generalist than the two specialists. These data both confirm the ecological significance of predators in the foraging behavior of herbivorous prey and demonstrate how sophisticated compensatory mechanisms allow foragers to partially offset the detrimental effects of reduced food intake. The fact that these mechanisms operated across a wide range of plant resistance phenotypes suggests that compensation is not always constrained by reduced food quality.     

Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment

A field experiment was conducted to examine the effect of perceived predation risk on the use of foraging areas by juvenile and adult primates under different conditions of local food abundance. Wild squirrel monkeys, Saimiri sciureus, were observed in an experiment conducted during the dry and the wet seasons at a site in Eastern Amazonia, Brazil. Animals were presented with feeding platforms that differed in food quantity and exposure to aerial predators through varying vegetative cover. In the dry season, juveniles and adults chose platforms based solely on food quantity. However, in the wet season, juveniles foraged preferentially on high-reward platforms only if cover level also was high (i.e., potentially offered greater concealment from predators). In contrast, adults showed the same pattern of platform use regardless of season. These results indicate that age and local resource availability based on seasonality affect whether primates forage in a predator-sensitive manner. Juveniles may be more sensitive to predation risk when foraging, and individuals may take fewer risks when resource abundance is high in their environment.     

Prey size affects the costs and benefits of group predation in nymphs of the predatory stink bug Andrallus spinidens (Heteroptera: Pentatomidae)

Group predation promotes foraging efficiency because it increases the size of prey that can be killed and improves hunting success compared to solitary predation. However, group predation may increase competition among group members during feeding. Earlier studies have focused on the advantages of group predation, but little is known about the costs and benefits of group predation for individual members of the group. Here, we show that the costs and benefits of group predation for individuals of the predatory stink bug Andrallus spinidens vary with prey size in laboratory experiments. We found that when A. spinidens fed on small prey, group predation did not significantly increase foraging efficiency but did increase competition for food among group members. In contrast, when prey was large, group predation promoted foraging efficiency, and competition over food was not detected. Our results suggest that group predation by A. spinidens nymphs is advantageous for individual members because it enables each member to hunt larger prey that could not be hunted alone. However, when group size was large or prey size was small, group predation increased competition among group members.     

Predation by squirrel monkeys and double-toothed kites on tent-making bats

Central American squirrel monkeys (Saimiri oerstedi) appear to recognize the modified leaves that phyllostomid bats utilize for diurnal roost sites. The monkeys visually and manually search these bat tents for both bats and insects. Adult males are the most successful at capturing bats. Nonvolant juvenile bats are more vulnerable to monkey predation than are adults. Bats that escape monkey predation frequently are captured by doubletoothed kites (Harpagus bidentatus) that tend foraging troops of monkeys. Predation by squirrel monkeys, coupled with that of double-toothed kites, may be a significant source of mortality for tent-making bats.     

Influence of environment structure and food availability on the foraging behaviour of the laboratory rat

According to the optimal foraging theory, an animal is expected to enter into a given activity depending on associated costs and benefits. In line with this assumption, numerous studies have suggested that energetic reward is balanced by predation risk in foraging decisions. Therefore, the use of information about indirect cues of predation risk such as physical structure (e.g. cover, escape substrate) can give individuals a selective advantage. We studied foraging behaviour in the laboratory rat in an experimental maze; it allowed us to vary two environmental parameters: food availability and physical structure. In a first experiment, rats were offered a choice between two areas only differing in cover density. In a second experiment, the two areas only differed in food density. In a third experiment, we crossed both parameters. Our results showed that high “cover” patch was preferentially exploited (experiment 1) and that rats foraged more in the high food density patch (experiment 2). The last experiment showed that rats partially trade-off between cover density and food availability, even if the safest area was still preferred. Therefore, we suggest that foraging decisions depend primarily on safety needs, rather than food availability, at least when animals are not severely food-deprived.     

The Impact of Physiological Demands on Foraging Decisions under Predation Risk: A Test with the Whelk Acanthina monodon

We study whether and how physiological demands affect foraging decisions under predation risk, by evaluating the effect of starvation on the rate of food consumption and prey‐size preferences and the potential trade‐off between starvation and predation risk on foraging behavior in the whelk Acanthina monodon, a gastropod inhabiting the intertidal rocky shores of central Chile. These whelks appear to adjust their foraging strategy to physiological (nutritional) demand and predation risk. Starvation reduced the effect of predation risk on the rate of food consumption by A. monodon. Thus, in the absence of the predator sea star, the rate of food consumption by starved and satiated whelks was similar. When a predator was present, starved whelks fed faster than satiated whelks. Our results indicate that foraging behaviour represents an integrated and hierarchical response to environmental conditions and the physiological conditions of the forager.     

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.     

Behavioural Response of Juvenile Bluegill Sunfish to Variation in Predation Risk and Food Level

The behavioural response of juvenile bluegill sunfish (Lepomis macrochirus) to predation risk when selecting between patches of artificial vegetation differing in food and stem density was investigated. Bluegill foraging activity was significantly affected by all three factors. Regardless of patch stem density or risk of predation bluegills preferred patches with the highest prey number. During each trial bluegill foraging activity was clearly divided into a between- and within-patch component. In the presence of a predator bluegills reduced their between-patch foraging activity by an equivalent amount regardless of patch stem density or food level, apparently showing a risk-adjusting behavioural response to predation risk. Within patches, however, foraging activity was affected by both food level and patch stem density. When foraging in a patch offering a refuge from predation, the presence of a predator had no effect on bluegill foraging activity within this patch. However, if foraging in a patch with only limited refuge potential, bluegill foraging activity was reduced significantly in the presence of a predator. Further, this reduction was significantly greater if the patch contained a low versus a high food level, indicating a risk-balancing response to predation with respect to within-patch foraging activity. Both these responses differ from the risk-avoidance response to predation demonstrated by juvenile bluegills when selecting among habitats. Therefore, our results demonstrate the flexibility of juvenile bluegill foraging behaviour.     

Axes of fear for stream fish: water depth and distance to cover

To better understand habitat-specific predation risk for stream fish, we used an approach that assumes animals trade off food for safety and accurately assess risk such that predation risk can be measured as a foraging cost: animals demand greater harvest rates to occupy riskier locations. We measured the foraging cost of predation risk for juvenile salmonids within enclosures in a natural stream at locations that varied in water depth and distance to cover. Measurements relied on a food delivery apparatus and direct observations that allowed estimation of “giving-up” harvest rates – food delivery rates at which animals left the feeding apparatus. Juvenile steelhead about 120 mm fork length exhibited sharp increases in giving-up harvest rate with decreasing water depth and refused to use the feeding device even when offered extreme food delivery rates in water ≤20 cm deep. Giving-up harvest rates were less affected by the distance to cover. Assuming the gradients we observed in giving-up harvest rates reflect predation risk, the results of this study can be applied to spatially explicit models of stream fish populations that incorporate risk into both habitat selection and mortality due to predation.