Lawrence M. Dill

The scent of death: Chemosensory assessment of predation risk by prey animals

AbstractIt 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 so...

Human-caused Disturbance Stimuli as a Form of Predation Risk

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, low- flying 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.

The Economics of Fleeing from Predators

Publisher Summary The chapter describes a simple economic model that predicts in a qualitative way on how costs (lost feeding opportunity and risk) interact to produce an optimal flight distance from approaching predators. Animals often defer the decision to flee from an approaching predator and continue with their ongoing activities. The view is that, a profitable approach to the problem of why such decisions are deferred, and how they are eventually made, is to view the process as an economic, one in which the relative costs of fleeing and staying change as a predator approaches. It is suggested that the economic approach will prove useful in analyzing many aspects of predator-prey interactions.

A DETERMINATION OF THE ENERGETIC EQUIVALENCE OF THE RISK OF PREDATION

The influence of predation risk on patch choice was measured by examining the spatial distribution of 10 guppies (Poecilia reticulata) between two feeders, at one of which there was a risk of predation. The distribution was assumed to be ideal free. Nine unique situations were examined using all possible combinations of three risk levels and three diet levels, for each sex of guppy separately. Both sex and diet level influenced the effect of predation risk on patch choice. For the females the effect of risk was highest at the intermediate diet level. However, the males exhibited the opposite response: the effect of risk of predation was lowest at the intermediate diet level. A simple equation was then used to predict how much extra food (representing the energetic equivalent of risk) must be added to the risky patch for the guppies to become indifferent to the risk differences between the two types of patches. This manipulation caused a similar number of guppies to use both the risky and safe feeders, reducing or offsetting the influence of risk of predation. However, the male guppies were less influenced by this manipulation than were the females. The different results for the two sexes are consistent with known differences in their life histories, indicating that a knowledge of an animals life history will often be necessary to

Risk of predation and the feeding behavior of juvenile coho salmon (Oncorhynchus kisutch)

SummaryDuring their first 1–2 years of life, juvenile coho salmon (Oncorhynchus kisutch) are stream-dwelling, and feed upon drifting invertebrates. They move upstream from a holding position to intercept individual prey items; the distance moved (attack distance) is an increasing, but decelerating, function of prey size. Since the fish are presumably more visible to predators during such feeding excursions, prey size and risk are associated variables.The effect on attack distance of the presentation of a model predator (a photograph of a rainbow trout) was examined in the laboratory. Attack distances are shortened following presentation of a predator; this is particularly true when the prey are large (Fig. 1). The extent of the reduction of attack distance is directly related to predator presentation frequency, although there appears to be a minimum level to which it will decline (Fig. 2). Hungry fish and fish in the presence of a competitor (simulated by a mirror) are less responsive to the predator, suggesting a trade-off of energetic requirements and risk (Fig. 3 and Table 3). The effect of predation risk should be to reduce the relative proportion of large prey in a juvenile cohos diet, and its net rate of energy intake.

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

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.

BEHAVIORALLY MEDIATED INDIRECT INTERACTIONS IN MARINE COMMUNITIES AND THEIR CONSERVATION IMPLICATIONS

The importance of density-mediated indirect effects (e.g., keystone predators) in marine communities has been widely recognized. Behaviorally mediated indirect interactions (BMIIs) may be equally important in marine systems, but have received relatively little attention. BMIIs occur when a change in an “initiator” species causes a behavioral shift in a “transmitter” species that, in turn, affects a “receiver” species. BMIIs between initiator and receiver species can be described by the ecological relationships between initiator and transmitter, and between transmitter and receiver (i.e., predator and prey, competitors, or no relationship), and the nature of the indirect effect on the receiver (i.e., positive or negative). We review published examples of BMIIs in marine communities, showing that BMIIs may create, enhance, ameliorate, or even reverse the sign of the direct interactions between species. Models that only include direct interactions or density-mediated indirect ones cannot predict some of thes...

Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics

1. Risk effects of predators can profoundly affect community dynamics, but the nature of these effects is context dependent. 2. Although context dependence has hindered the development of a general framework for predicting the nature and extent of risk effects, recent studies suggest that such a framework is attainable if the factors that shape anti-predator behaviour, and its effectiveness, in natural communities are well understood. 3. One of these factors, the interaction of prey escape tactics and landscape features, has been largely overlooked. 4. We tested whether this interaction gives rise to interspecific variation in habitat-use patterns of sympatric large marine vertebrates at risk of tiger shark (Galeocerdo cuvier Peron and LeSueur, 1822) predation. Specifically, we tested the a priori hypothesis that pied cormorants (Phalacrocorax varius Gmelin, 1789) would modify their use of shallow seagrass habitats in a manner opposite to that of previously studied dolphins (Tursiops aduncus Ehrenberg, 1833), dugongs (Dugong dugon Müller, 1776), and green turtles (Chelonia mydas Linnaeus, 1758) because, unlike these species, the effectiveness of cormorant escape behaviour does not vary spatially. 5. As predicted, cormorants used interior and edge portions of banks proportional to the abundance of their potential prey when sharks were absent but shifted to interior portions of banks to minimize encounters with tiger sharks as predation risk increased. Other shark prey, however, shift to edge microhabitats when shark densities increase to take advantage of easier escape despite higher encounter rates with sharks. 6. The interaction of landscape features and escape ability likely is important in diverse communities. 7. When escape probabilities are high in habitats with high predator density, risk effects of predators can reverse the direction of commonly assumed indirect effects of top predators. 8. The interaction between landscape features and prey escape tactics can result in a single predator species having differential effects on their sympatric prey that could cascade through ecosystems and should be incorporated into a general framework for context dependence of risk effects.

MORTALITY RISK VS. FOOD QUALITY TRADE-OFFS IN A COMMON CURRENCY: ANT PATCH PREFERENCES'

Many studies have shown that predation risk affects foraging behavior, but quantitative predictions are rare because of the lack of a common currency for energy intake and mortality. This problem is soluble in ants. We gave 12 Lasius pallitarsis colonies the choice between foraging in two patches that differed both in food quality and in associated mortality risk. We independently measured the growth that colonies could achieve on the diets offered in those patches. With no risk at either patch, colonies always preferred the higher food quality patch. When mortality risk (a large Formica subnuda ant) was associated with the trail to the higher food quality patch, the use of that patch depended on the magnitude of the growth differential between feeding in risky or safe patches: the greater the benefit of feeding in the risky patch, the greater was its relative usage. Colonies valued risky patches equally to safe patches at the point where forager mortality rates were approximately offset by colony growth gain. This ability to reduce mortality risk while foraging may be a factor that favors insect sociality, in general.

The energetics of feeding territoriality in juvenile coho salmon (Oncorhynchus kisutch)

1. A foraging time budget was developed for territorial, nonterritorial, and floater fish. Territorial fish spend 76% of total time at the station, 3% free swimming, 13% feeding, and 5 % in agonistic activity. Floaters spend 18% of their time stationary swimming, 54% free swimming, 10% feeding, and 10% in agonistic activity. Nonterritorial fish spend 50% of their time stationary swimming, 43% free swimming, 2% feeding, and 3% in agonistic activity. 2. Stationary swimming tailbeat frequency for the floater (4.3) is significantly higher than for the territorial fish (3.6). The floater flight tailbeat frequency (8.2) is significantly higher than the territorial chase tailbeat frequency (6.9). Normal feed tailbeat frequencies are similar for all fish groups. Nonterritorial fish tend to move slowly (tailbeat frequency = 3.3) for all activities except normal feed. 3. The total activity budgets for territorial, floater, and nonterritorial fish are 1199, 1318, and 910 cal/kg/hr, respectively. The territorial fish uses 91 % as many calories as the floater fish and the nonterritorial fish utilizes 76% of the territorial budget. 4. Total agonistic costs represent 12 and 14% of the territorial and floater fish activity budgets, respectively. 5. The costs per feeding motion for the territorial, floater, and nonterritorial fish are 4.03, 4.91, 10.1 cal/motion, respectively. 6. The territorial fish has a net energy intake advantage over the floater, and probably over the nonterritorial fish, due to 1) reduced search costs, 2) reduced prey pursuit costs, and 3) reduced agonistic activity costs.