Steven L. Lima

Stress and Decision Making under the Risk of Predation: Recent Developments from Behavioral, Reproductive, and Ecological Perspectives

Publisher Summary This chapter reviews the present empirical and theoretical work on antipredator decision making. The ways in which predators influence the behavioral decisions made by their prey is now the subject of a large and growing literature. Some notable recent advances include clear demonstrations that antipredatory decision making (1) may influence many aspects of reproductive behavior, (2) has demonstrable long-term consequences for individual fitness, and (3) may influence the nature of ecological systems themselves. There have also been many advances in the theory of antipredator behavior, which should provide a sound conceptual basis for further progress. Attention is needed for further work on the effects that predator and prey have on the others behavioral decisions. The range of reproductive behaviors influenced by the risk of predation also requires much more investigation. Work on the long-term costs of antipredator decision making needs more empirical documentation and greater taxonomic diversity. Work on the ecological implications of antipredatory decision making has only scratched the surface, especially with regard to population-level effects and species interactions. Theoretical investigations should also play a prominent role in future work.

Towards a behavioral ecology of ecological landscapes

Recent developments in landscape-level ecological modeling rest upon poorly understood behavioral phenomena. Surprisingly, these phenomena include animal movement and habitat selection, two areas with a long history of study in behavioral ecology. A major problem in applying traditional behavioral ecology to landscape-level ecological problems is that ecologists and behaviorists work at very different spatial scales. Thus a behavioral ecology of ecological landscapes would strive to overcome this inopportune differential in spatial scales. Such a landscape-conscious behavioral undertaking would not only establish more firmly the link between behavior and ecological systems, but also catalyze the study of basic biological phenomena of Interest to behaviorists and ecologists alike.

PREDATION RISK AND UNPREDICTABLE FEEDING CONDITIONS: DETERMINANTS OF BODY MASS IN BIRDS'

The body mass (or fat reserves) maintained by a wintering bird can be viewed as a trade-off between the risk of starvation and the risk of predation. This follows from the fact that fat reserves affect survival in very different ways. From the starvation point of view, a bird should be as fat (or heavy) as possible in order to minimize its probability of starvation during weather-related food unavailability because fatter birds can survive longer without food than leaner birds. From the predation risk point of view, however, a bird should be as lean as possible to minimize its probability of being killed. Leaner birds will incur a smaller cost of existence than heavier birds and thus spend less time feeding, potentially exposed to predators. In addition, lean birds are likely to be more adept at escaping predators once attacked. If a bird is attempting to minimize its probability of death during the winter season, the fat reserves and thus the body mass it maintains will reflect a trade-off between starvation and predation risk. A simple stochastic simulation model developed to explore the nature of this trade-off indicates that body mass should: (1) increase with the frequency and/or harshness of periods of food unavailability (due to snow, ice, wind, etc.); (2) decrease with increasing predation risk; (3) decrease with increasing temperature; and (4) increase with food abundance. The analysis of the model readily explains why wintering birds maintain fat levels lower than those of which they are capable. The tendency for individuals of a given bird species to be heavier in more northerly populations and during midwinter is also readily interpreted in terms of the above trade- off. Implications for foraging behavior and population regulation in wintering birds are discussed.

Back to the basics of anti-predatory vigilance: the group-size effect

Abstract A negative relationship between group size and levels of individual vigilance is widespread in socially feeding vertebrates. The main explanation of this ‘group-size effect’, the many-eyes hypothesis, is based on the simple premise that as group size increases, there are progressively more eyes scanning the environment for predators. Thus an individual forager can devote less time to vigilance (and more time to feeding) as group size increases without any lessening of the groups ability to detect an attack. Basic to this hypothesis is the assumption of collective detection: that all members of the group are alerted to an attack as long as it is detected by at least one individual. In addition, an important presumption associated with the many-eyes hypothesis is that individuals monitor the vigilance behaviour of their groupmates in determining their own level of vigilance. Neither the idea of collective detection nor behavioural monitoring received strong support in an experimental study of vigilance in mixed flocks of dark-eyed juncos, Junco hyemalis, and American tree sparrows, Spizella arborea. The lack of support for behavioural monitoring was particularly evident; however, some degree of collective detection was apparent. It is possible that anti-predatory rules-of-thumb may explain the group-size effect while keeping intact the basics of the many-eyes hypothesis.

Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation

A growing body of work suggests that breeding birds have a significant capacity to assess and respond, over ecological time, to changes in the risk of predation to both themselves and their eggs or nestlings. This review investigates the nature of this flexibility in the face of predation from both behavioural and reproductive perspectives, and also explores several directions for future research.

Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep

Several animals mitigate the fundamental conflict between sleep and wakefulness by engaging in unihemispheric sleep, a unique state during which one cerebral hemisphere sleeps while the other remains awake. Among mammals, unihemispheric sleep is restricted to aquatic species (Cetaceans, eared seals and manatees). In contrast to mammals, unihemispheric sleep is widespread in birds, and may even occur in reptiles. Unihemispheric sleep allows surfacing to breathe in aquatic mammals and predator detection in birds. Despite the apparent utility in being able to sleep unihemispherically, very few mammals sleep in this manner. This is particularly interesting since the reptilian ancestors to mammals may have slept unihemispherically. The relative absence of unihemispheric sleep in mammals suggests that a trade off exists between unihemispheric sleep and other adaptive brain functions occurring during sleep or wakefulness. Presumably, the benefits of sleeping unihemispherically only outweigh the costs under extreme circumstances such as sleeping at sea. Ultimately, a greater understanding of the reasons for little unihemispheric sleep in mammals promises to provide insight into the functions of sleep, in general.

Sleeping under the risk of predation.

Every studied animal engages in sleep, and many animals spend much of their lives in this vulnerable behavioural state. We believe that an explicit description of this vulnerability will provide many insights into both the function and architecture (or organization) of sleep. Early studies of sleep recognized this idea, but it has been largely overlooked during the last 20 years. We critically evaluate early models that suggested that the function of sleep is antipredator in nature, and outline a new model in which we argue that whole-brain or ‘blackout’ sleep may be the safest way to sleep given a functionally interconnected brain. Early comparative work also suggested that the predatory environment is an important determinant of sleep architecture. For example, species that sleep in risky environments spend less time in the relatively vulnerable states of sleep. Recent experimental work suggests that mammals and birds shift to relatively vigilant (lighter) states of sleep in response to an increase in perceived risk; these results mirror the influence of stress on sleep in humans and rats. We also outline a conceptual model of sleep architecture in which dynamic changes in sleep states reflect a trade-off between the benefits of reducing a sleep debt and the cost of predation. Overall, many aspects of plasticity in sleep related to predation risk require further study, as do the ways in which sleeping animals monitor predatory threats. More work outside of the dominant mammalian paradigm in sleep is also needed. An ecologically based view of sleeping under the risk of predation will provide an important complement to the traditional physiological and neurological approaches to studying sleep and its functions.

Clutch size in birds: a predation perspective

A simple model of clutch size in nidicolous birds is developed in which the cost of reproduction is the risk of predation to both the parent and its dependent young. An analysis of the model shows that (1) conventional ideas of food limitation, though sufficient, are not necessary for the existence of an optimal clutch size; (2) predation as the sole cost of reproduction is adequate for the existence of an optimal clutch size; and (3) one need not expect a clutch-size-dependent physiological cost to a parent (leading to increased mortality) to be a major determinant of clutch size. In addition, several exper- imental and observational results that purport to demonstrate food limitation in breeding birds are also consistent with the idea of predation risk as the major cost of reproduction. Current ideas of clutch size determination and the costs of reproduction are considered in light of the above results, and possible syntheses are suggested. A predation-risk perspective may offer considerable insight into the evolution of clutch size in birds.

Half-Awake to the Risk of Predation

Birds have overcome the problem of sleeping in risky situations by developing the ability to sleep with one eye open and one hemisphere of the brain awake. Such unihemispheric slow-wave sleep is in direct contrast to the typical situation in which sleep and wakefulness are mutually exclusive states of the whole brain. We have found that birds can detect approaching predators during unihemispheric slow-wave sleep, and that they can increase their use of unihemispheric sleep as the risk of predation increases. We believe this is the first evidence for an animal behaviourally controlling sleep and wakefulness simultaneously in different regions of the brain.

Landscape-Level Perceptual Abilities in White-Footed Mice: Perceptual Range and the Detection of Forested Habitat

We define perceptual range as the distance from which an animal can perceive key landscape elements, such as distant patches of forested habitat. We argue that perceptual range should be a determinant of not only dispersal success in unfamiliar or hostile landscapes, but also of several landscape-level ecological processes influencing population dynamics. To redress the absence of empirical information on perceptual ranges, we simulated the dispersal of forest-dwelling white-footed mice (Peromyscus leucopus) across an agricultural landscape by releasing mice into unfamiliar, hostile agricultural habitat at various distances from fragments of forested habitat. We found that these forest mice have a remarkably low perceptual range with regard to detecting their forested (core) habitat. Mice released into bare fields failed to even orient towards forested habitat as little as 30 m distant, while mice in crop fields appeared unable to locate forest habitat as little as 10 m distant. These mice seemed to locate forested habitat by vision, despite the availability of non-visual cues. Future work will undoubtedly demonstrate vast differences in landscape-level perceptual abilities among animals, and show clearly that the ecological effects of a given landscape configuration will be influenced by the behavioral attributes of the species in question.