Stress and Decision Making under the Risk of Predation: Recent Developments from Behavioral, Reproductive, and Ecological Perspectives
Introduction
My objective here is to provide a comprehensive review of recent 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. This sustained interest in the behavioral aspects of predator–prey interactions is readily traced to the fact that virtually all animals are subjected to some form of predation, and many biological and ecological insights can be gained from an understanding of the ways in which predators influence their prey's behavior.
Prey decision making under the risk of predation essentially allows an animal to manage predator-induced stress. Stress is not a term commonly associated with the study of antipredator decision making, but this is largely a matter of semantics, and one can relate stress to such decision making in several contexts. If one defines stress as an environmental condition that diminishes Darwinian fitness through either reproduction or survival (e.g., Sibly and Calow, 1989), then few aspects of an environment would lead to more stress than predators. Note that death due to predation is not the sort of stress that I consider here; observable predator-induced stress in animals is (in part) a result of prey decision making itself, such as the energetic stress caused by choosing to feed less in the presence of predators. One might thus consider the adaptive management of this sort of predator-induced stress as a main function of antipredator decision making. Forms of non-predator-induced stress, such as energetic stress caused by food shortages, will also influence such decision making. This view of stress is ecological or evolutionary in perspective, and most of the existing literature deals with stress in this context.
A more classical definition of stress concerns the rapid increase in certain hormones (e.g., glucocorticoids) in response to some threatening situation (Weiner, 1992). This hormonal response is considered to be a biological marker of fear (Boissy, 1995), and there exists a substantial literature on fear and the physiological (neuroendocrine) stress response (for a review, see Boissy, 1995). However, relatively few studies on physiological stress have worked with predators, and research relating such stress to antipredator behavior is still in its infancy (Bercovitch et al., 1995; Boissy, 1995). Further research into these physiological aspects of stress may ultimately have several important implications for how we view antipredator decision making, several of which I summarize in a closing section.
Regardless of the topic being addressed, all of the published works included in this review share certain characteristics. First, the behaviors/decisions in question respond in ecological time to changes in some component of the risk of predation (sensu Lima and Dill, 1990). That is, this review concerns plastic behavioral traits that respond to short-term perceived changes in the risk of predation. Thus, I do not consider in detail those aspects of behavior that respond to predation over evolutionary time (see Edmunds, 1974; Endler, 1991). Second, figuring prominently in most studies included herein is the inevitable trade-off between the benefits of avoiding possible predation and the costs of doing so, in terms of feeding, survival, or reproduction (i.e., stresses as defined earlier). Third, for reasons of manageability, I include work published primarily during the last 7–8 years. This covers roughly the time period since the publication of several relevant reviews that were written in the late 1980s (Dill, 1987; Sih, 1987; Lima and Dill, 1990). The present review nevertheless encompasses about twice the number of papers covered by Lima and Dill (1990), whose comprehensive coverage extended over almost a 15-year period!
I have strived to provide perspectives on antipredator decision making that encompass several levels of biological organization. I thus cover the spectrum from short-term decision making by individuals to the consequences of such decision making for long-term fitness, population dynamics, and species interactions. Work on short-term decision making under the risk of predation has a relatively long history of study (Milinski, 1986; Sih, 1987; Lima and Dill, 1990), whereas most of the work on its consequences has appeared in recent years. My choices for the topics organizing this review reflect an attempt to provide a representative perspective on the current state of the field—I hope they succeed. In the hope of synthesizing available studies as much as possible, I have also classified studies across several topics to the extent warranted.
Section snippets
Behavior of Feeding Animals: Classical Motivations
It is appropriate to begin with an examination of recent empirical and theoretical work on foraging behavior. By “classical,” I refer to studies motivated directly or historically by optimal foraging theory (Stephens and Krebs, 1986). Work in this area still forms the main empirical, theoretical, and philosophical basis for the study of decision making under the risk of predation. Note that while this section focuses mainly on classical issues, subsequent sections often deal with the behavior
Patterns of Activity
“Activity” studies examine the influence of predators on both the level and the temporal patterning of prey activity. I consider each of these areas in turn. These studies on prey activity provide some of the best documented behavioral responses by prey to the presence of predators, and form the foundation for much behaviorally explicit ecological research on predator-prey interactions (e.g., Werner, 1992; Wooster and Sih, 1995).
After an Encounter with a Predator
Recent work on postencounter decision making covers a variety of topics, such as the resumption of activity, the choice of escape behavior, and flight initiation distance. In covering these topics, I focus on behavior that is flexible with respect to changes in the predatory environment; papers describing simple evasive behaviors in response to attack are outside the scope of this review.
Adaptive Sociality
Decision making by individuals ought to influence the nature of sociality under the risk of predation (e.g., Pulliam and Caraco, 1984). The last few years have seen considerable progress in the study of such decision making, but there are still surprisingly few studies in this area (see also Lima and Dill, 1990; Krause, 1994b). Recent years have also seen advances in the comparative study of predation and sociality (notably in primates; e.g., Boesch, 1991; Cowlishaw, 1994; van Schaik and
Reproduction
Sih (1994) summarizes the current state of affairs with regard to reproductive decision making under the risk of predation: “Although predation risk is often viewed as an important component … of the evolution of mating behavior, … little effort has gone into gaining a deep, ecologically-rooted understanding of how predation risk influences reproductive behavior.” A similar sentiment is expressed in Lima and Dill (1990), Magnhagen (1991, 1993), and Reynolds (1993). Recent years have nonetheless
Long-Term Consequences of Decision Making
Most studies on antipredatory decision making accept the idea that any decision has associated with it both a fitness cost (some form of predator-induced stress) and benefit (avoiding an early death). How much do we really know about these issues?
There are now several studies demonstrating that antipredator decision making does indeed lower an animal's risk of predation (as per examples mentioned throughout this review). However, such benefits of antipredator decision making remain a
Ecological Influences and Implications
Decision making under the risk of predation can influence the nature of ecological systems. Understanding these influences has long been a major driving force in the study of antipredator decision making (Sih, 1980; Werner et al., 1983). Here, I discuss recent work in this area within three main contexts: the use of space by individuals, population-level consequences, and species interactions. This work involves mostly field or semifield experimentation. Although often not achieving the
Additional Considerations
In this section I group four disparate topics about which relatively little is known. These topics nonetheless address several important issues in the study of decision making under the risk of predation.
Conclusions and Summary
Recent years have witnessed increasing interest in the study of antipredatory decision making and its consequences. This recent work is much too vast to summarize in detail, but 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
Acknowledgments
I thank Peter Slater. Manfred Milinski, and Anders Møller for their comments on the manuscript, and their efforts regarding this volume on stress and behavior. Peter Bednekoff and Patrick Zollner also commented on the manuscript. Chris Mathews provided competent assistance with the literature search. Hilary Philpot helped in the preparation of the References section. Finally, much of the background work in preparing this review was made possible by a sabbatical leave granted by Indiana State
References (537)
Alertness signalling in two rail species
Anim. Behav.
(1993)The effect of body condition of the trade-off between vigilance and foraging in Belding's ground squirrels
Anim. Behav.
(1993)- et al.
The endocrine stress response and alarm vocalizations in rhesus macaques
Anim. Behav.
(1995) Pregnancy incentives, predation constraints and habitat shifts: Experimental and field evidence for wild bighorn sheep
Anim. Behav.
(1991)Risky sex: Male pipefishes mate at random in the presence of a predator
Anim. Behav.
(1993)- et al.
The effects of food, predation risk and endogenous rhythmicity on the behaviour of juvenile plaice, Pleuronectes platessa L
Anim. Behav.
(1995) Pursuit-deterrence revisited
Trends Ecol. Evol.
(1995)- et al.
Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish
Anim. Behav.
(1994) Flocking is an effective anti-predation strategy in redshanks
Tringa totanus. Anim. Behav.
(1994)- et al.
Effects of food supply, hunger, danger and competition on choice of foraging location by the fifteen-spined stickleback, Spinachia spinachia L
Anim. Behav.
(1991)