Predation has long been implicated as a major selective force in the evolution of several morphological and behavioral characteristics of animals. The importance of predation during evolutionary time is clear, but growing evidence suggests that animals also have the ability to assess and behaviorally influence their risk of being preyed upon in ecological time (i.e., during their lifetime). We develop an abstraction of the predation process in which several components of predation risk are identified. A review of the literature indicates that an animal's ability to assess and behaviorally control one or more of these components strongly influences decision making in feeding animals, as well as in animals deciding when and how to escape predators, when and how to be social, or even, for fishes, when and how to breathe air. This review also reveals that such decision making reflects apparent trade-offs between the risk of predation and the benefits to be gained from engaging in a given activity. Despite this body of evidence, several areas in the study of animal behavior have received little or no attention from a predation perspective. We identify several such areas, the most important of which is that dealing with animal reproduction. Much work also remains regarding the precise nature of the risk of predation and how it is actually perceived by animals, and the extent to which they can behaviorally control their risk of predation. Mathematical models will likely play a major role in future work, and we suggest that modelers strive to consider the potential complexity in behavioral responses to predation risk. Overall, since virtually every animal is potential prey for others, research that seriously considers the influence of predation risk will provide significant insight into the nature of animal behavior.
ABSTRACT. A growing number of studies quantify the impact of nonlethal human disturbance on the behavior and reproductive success of animals. Athough many are well designed and analytically sophisticated, most lack a theoretical framework for making predictions and for understanding why particular responses occur. Behavioral ecologists have recently begun to fill this theoretical vacuum by applying economic models of antipredator behavior to disturbance studies. In this emerging paradigm, predation and nonlethal disturbance stimuli create similar trade-offs between avoiding perceived risk and other fitness-enhancing activities, such as feeding, parental care, or mating. A vast literature supports the hypothesis that antipredator behavior has a cost to other activities, and that this trade-off is optimized when investment in antipredator behavior tracks short-term changes in predation risk. Prey have evolved antipredator responses to generalized threatening stimuli, such as loud noises and rapidly approaching objects. Thus, when encountering disturbance stimuli ranging from the dramatic, lowflying helicopter to the quiet wildlife photographer, animal responses are likely to follow the same economic principles used by prey encountering predators. Some authors have argued that, similar to predation risk, disturbance stimuli can indirectly affect fitness and population dynamics via the energetic and lost opportunity costs of risk avoidance. We elaborate on this argument by discussing why, from an evolutionary perspective, disturbance stimuli should be analogous to predation risk. We then consider disturbance effects on the behavior of individuals-vigilance, fleeing, habitat selection, mating displays, and parental investment-as well as indirect effects on populations and communities. A wider application of predation risk theory to disturbance studies should increase the generality of predictions and make mitigation more effective without over-regulating human activities.
It is well documented that animals take risk of predation into account when making decisions about how to behave in particular situations, often trading-off risk against opportunities for mating or acquiring energy. Such an ability implies that animals have reliable information about the risk of predation at a given place and time. Chemosensory cues are an important source of such information. They reliably reveal the presence of predators (or their presence in the immediate past) and may also provide information on predator activity level and diet. In certain circumstances (e.g., in the dark, for animals in hiding) they may be the only cues available. Although a vast literature exists on the responses of prey to predator chemosensory cues (or odours), these studies are widely scattered, from marine biology to biological control, and not well known or appreciated by behavioural ecologists. In this paper, we provide an exhaustive review of this literature, primarily in tabular form. We highlight some of the more representative examples in the text, and discuss some ecological and evolutionary aspects of the use of chemosensory information for prey decision making. Curiously, only one example illustrates the ability of birds to detect predator odours and we have found no examples for terrestrial insects, suggesting a fruitful area for future study.Résumé : Il est bien connu qu'un animal qui doit prendre une décision d'ordre comportemental prend en considération le risque de prédation associé à cette décision. Souvent, l'animal passera outre ce risque pour se reproduire ou se nourrir. Une telle habilité implique que l'animal a une information spatio-temporelle valable sur le risque de prédation. Les indices chimiques constituent une source importante d'informations. Ils révèlent la présence de prédateurs (où leur passage récent) et donnent des renseignements sur le taux d'activité du prédateur et sur sa diète. Dans certaines circonstances (dans l'obscurité ou en présence de prédateurs chassant à l'affût), les indices chimiques peuvent être les seuls permettant aux proies de détecter leurs prédateurs. Il existe une littérature abondante sur la réponse des proies aux indices chimiques (ou odeurs) fournis par les prédateurs. Ces travaux sont néanmoins disparates (leurs sujets s'étendent de la biologie marine au contrôle biologique), peu connus et peu appréciés des écologistes spécialistes de l'étude des comportements. Dans cet article, nous faisons une revue exhaustive de cette littérature, notamment sous la forme de tableaux. Nous mettons en relief dans le texte les exemples les plus représentatifs. Nous discutons aussi des aspects écologiques et évolutifs reliés à l'utilisation des informations chimiques par les proies lors de prises de décisions. Curieusement, un seul exemple illustre l'habilité des oiseaux à la détection des odeurs des prédateurs. Nous n'avons pas trouvé d'exemple chez les insectes terrestres. Il y a donc là un terrain potentiellement fructueux pour de futurs travaux.
We develop a model to predict position choice of drift-feeding stream salmonids, assuming a fish chooses the position that maximizes its net energy intake rate. The fish's habitat is represented as a series of stream cross-profiles, each divided into vertical strips characterized by water depth and velocity. The fish may select a focal point in any of these strips, and include several neighbouring strips in its foraging area. The number of prey the fish encounters depends on its reaction distance to prey, water depth, and water velocity; the proportion of detected prey the fish is able to capture declines with water velocity. The fish's net energy intake rate is its gross energy intake rate from feeding minus the swimming cost calculated by using water velocity at the fish's focal point. There was a close match between the positions predicted by this model and those chosen by solitary Arctic grayling (Thymallus arcticus) in the pools of a mountain stream in Alaska.
Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.
Summary 1.A predictive framework of community and ecosystem dynamics that applies across systems has remained elusive, in part because non-consumptive predator effects are often ignored. Further, it is unclear how much individual-level detail community models must include. 2. Previous studies of short-lived species suggest that state-dependent decisions add little to our understanding of community dynamics. Body condition-dependent decisions made by long-lived herbivores under risk of predation, however, might have greater communitylevel effects. This possibility remains largely unexplored, especially in marine environments. 3. In the relatively pristine seagrass community of Shark Bay, Australia, we found that herbivorous green sea turtles ( Chelonia mydas Linnaeus, 1758) threatened by tiger sharks ( Galeocerdo cuvier Peron and LeSueur, 1822) select microhabitats in a conditiondependent manner. Turtles in poor body condition selected profitable, high-risk microhabitats, while turtles in good body condition, which are more abundant, selected safer, less profitable microhabitats. When predation risk was low, however, turtles in good condition moved into more profitable microhabitats. 4. Condition-dependent use of space by turtles shows that tiger sharks modify the spatiotemporal pattern of turtle grazing and their impacts on ecosystem dynamics (a traitmediated indirect interaction). Therefore, state-dependent decisions by individuals can have important implications for community dynamics in some situations. 5. Our study suggests that declines in large-bodied sharks may affect ecosystems more substantially than assumed when non-lethal effects of these top predators on mesoconsumers are not considered explicitly.
Flexibility is an important adaptive feature of the foraging behavior of fishes, because most natural environments vary both spatially and temporally. Fish should respond to low levels of food availability by altering their behavior in ways which ensure higher feeding rates, larger feeding territories, and broader diets. It is shown that the gastric sensation of hunger and its rate of change may act as appropriate cues to food availability, and observed hunger-motivated changes in feeding behavior can produce all of these predicted effects. Data are presented to show that juvenile coho salmon (Oncorhynchus kisutch) alter their behavior in an adaptive manner when faced with variable degrees of threat of competition from territorial intruders, and of risk of predation. A review of similar studies on other species supports the generality of these results. Learning is an important mechanism providing behavioral flexibility, and changes in fish feeding behavior with experience are summarized. A graphical model is developed to show that these changes can result in training biases and food specialization. Learning also results in increased feeding rates. The consequences of these observations for the development of refined models of foraging are discussed.
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