Social buffering in a eusocial invertebrate: termite soldiers reduce the lethal impact of competitor cues on workers.

While the impact of predator-induced stress on prey has received considerable attention, there has been far less research into the effect of competitors. Cues from aggressive competitors should be particularly likely to evoke behavioral and/or physiological responses, since they may be indicative of both direct (interference) and indirect (exploitative) threats. The danger posed by such competitors, and the "fear" they evoke, should be reduced at lower competitor densities and by the presence of individual conspecifics specialized for defense. We assessed how Reticulitermes flavipes termite workers and soldiers were affected by cues from conspecific nestmates, conspecific non-nestmates, and the heterospecific competitor R. virginicus. Competitor cues altered flavipes worker and soldier behavior, decreasing worker growth and increasing their mortality. The presence of flavipes soldiers largely ameliorated these negative impacts: adding even a single soldier (5% of flavipes individuals) decreased worker mortality by 50-80%. Although worker mortality increased with competitor density, increased soldier densities did not increase the benefit to workers. The small number of soldiers required to substantially alter cue-mediated interactions suggests that this caste, in addition to providing direct defense, also occupies a "keystone role" by providing homeostatic feedback to workers functioning in stressful environments.

Human activities change marine ecosystems by altering predation risk.

In ocean ecosystems, many of the changes in predation risk - both increases and decreases - are human-induced. These changes are occurring at scales ranging from global to local and across variable temporal scales. Indirect, risk-based effects of human activity are known to be important in structuring some terrestrial ecosystems, but these impacts have largely been neglected in oceans. Here, we synthesize existing literature and data to explore multiple lines of evidence that collectively suggest diverse human activities are changing marine ecosystems, including carbon storage capacity, in myriad ways by altering predation risk. We provide novel, compelling evidence that at least one key human activity, overfishing, can lead to distinct, cascading risk effects in natural ecosystems whose magnitude exceeds that of presumed lethal effects and may account for previously unexplained findings. We further discuss the conservation implications of human-caused indirect risk effects. Finally, we provide a predictive framework for when human alterations of risk in oceans should lead to cascading effects and outline a prospectus for future research. Given the speed and extent with which human activities are altering marine risk landscapes, it is crucial that conservation and management policy considers the indirect effects of these activities in order to increase the likelihood of success and avoid unfortunate surprises.

A framework and standardized terminology to facilitate the study of predation-risk effects.

The very presence of predators can strongly influence flexible prey traits such as behavior, morphology, life history, and physiology. In a rapidly growing body of literature representing diverse ecological systems, these trait (or "fear") responses have been shown to influence prey fitness components and density, and to have indirect effects on other species. However, this broad and exciting literature is burdened with inconsistent terminology that is likely hindering the development of inclusive frameworks and general advances in ecology. We examine the diverse terminology used in the literature, and discuss pros and cons of the many terms used. Common problems include the same term being used for different processes, and many different terms being used for the same process. To mitigate terminological barriers, we developed a conceptual framework that explicitly distinguishes the multiple predation-risk effects studied. These multiple effects, along with suggested standardized terminology, are risk-induced trait responses (i.e., effects on prey traits), interaction modifications (i.e., effects on prey-other-species interactions), nonconsumptive effects (i.e., effects on the fitness and density of the prey), and trait-mediated indirect effects (i.e., the effects on the fitness and density of other species). We apply the framework to three well studied systems to highlight how it can illuminate commonalities and differences among study systems. By clarifying and elucidating conceptually similar processes, the framework and standardized terminology can facilitate communication of insights and methodologies across systems and foster cross-disciplinary perspectives.

Landscapes of Fear: Spatial Patterns of Risk Perception and Response.

Animals experience varying levels of predation risk as they navigate heterogeneous landscapes, and behavioral responses to perceived risk can structure ecosystems. The concept of the landscape of fear has recently become central to describing this spatial variation in risk, perception, and response. We present a framework linking the landscape of fear, defined as spatial variation in prey perception of risk, to the underlying physical landscape and predation risk, and to resulting patterns of prey distribution and antipredator behavior. By disambiguating the mechanisms through which prey perceive risk and incorporate fear into decision making, we can better quantify the nonlinear relationship between risk and response and evaluate the relative importance of the landscape of fear across taxa and ecosystems.

Indirect risk effects reduce feeding efficiency of ducks during spring.

Indirect risk effects of predators on prey behavior can have more of an impact on prey populations than direct consumptive effects. Predation risk can elicit more vigilance behavior in prey, reducing the amount of time available for other activities, such as foraging, which could potentially reduce foraging efficiency. Understanding the conditions associated with predation risk and the specific effects predation risk have on prey behavior is important because it has direct influences on the profitability of food items found under various conditions and states of the forager. The goals of this study were to assess how ducks perceived predation risk in various habitat types and how strongly perceived risk versus energetic demand affected foraging behavior. We manipulated food abundance in different wetland types in Illinois, USA to reduce confounding between food abundance and vegetation structure. We conducted focal-animal behavioral samples on five duck species in treatment and control plots and used generalized linear mixed-effects models to compare the effects of vegetation structure versus other factors on the intensity with which ducks fed and the duration of feeding stints. Mallards fed more intensively and, along with blue-winged teal, used longer feeding stints in open habitats, consistent with the hypothesis that limited visibility was perceived to have a greater predation risk than unlimited visibility. The species temporally nearest to nesting, wood ducks, were willing to take more risks for a greater food reward, consistent with an increase in a marginal value of energy as they approached nesting. Our results indicate that some duck species value energy differently based on the surrounding vegetation structure and density. Furthermore, increases in the marginal value of energy can be more influential than perceived risk in shaping foraging behavior patterns. Based on these findings, we conclude that the value of various food items is not solely determined by energy contained in the item but by conditions in which it is found and the state of the forager.

Antioxidant Enzyme Activities Vary with Predation Risk and Environmental Conditions in Free-Living Passerine Birds.

Prolonged physiological stress response may lead to an excessive production of reactive oxygen species (ROS) and ultimately to oxidative stress and severe fitness costs. We investigated whether natural variation in predation risk, induced by pygmy owls (Glaucidium passerinum), modifies the oxidative status of two free-living food-supplemented passerine bird species-the great tit (Parus major) and the willow tit (Poecile montanus)-in March 2012 and 2013. Predation risk significantly affected antioxidant enzyme activities of willow tits. Antioxidant enzyme activities (principal component factor 2 [PC2] representing glutathione-S-transferase and superoxide dismutase activities) were higher in high predation risk areas in 2013 than in low predation risk areas in the same year. Higher enzyme activities may suggest higher ROS production in birds living under high predation risk. In addition, antioxidant enzyme activities (PC2) were also higher in high predation risk areas in 2013 than in high predation risk areas in the previous year, 2012. This may represent variation in the risk represented by pygmy owls, which is probably inversely related to the natural fluctuations in the densities of their main prey, voles. In willow tits, PC1 (representing catalase, total glutathione, the ratio of reduced to oxidized glutathione, and protein carbonylation) was not affected by perceived predation risk, nor were antioxidant levels or enzyme activities in great tits. Higher enzyme activities observed in willow tits suggest that predator presence can modify the antioxidant status of avian prey, but the response also seem to be influenced by other environmental characteristics, like harsh winter conditions.

Cooccurrence of prey species alters the impact of predators on prey performance through multiple mechanisms.

When prey are differentially affected by intra and interspecific competition, the cooccurrence of multiple prey species alters the per capita availability of food for a particular prey species which could alter how prey respond to the threat of predation, and hence the overall-effect of predators. We conducted an experiment to examine the extent to which the nonconsumptive and overall effect of predatory water bugs on snail and tadpole traits (performance and morphology) depended on whether tadpoles and snails cooccurred. Tadpoles and snails differed in their relative susceptibility to intraspecific and interspecific competition, and predators affected both prey species via consumptive and nonconsumptive mechanisms. Furthermore, the overall effect of predators often depended on whether another prey species was present. The reasoning for why the overall effect of predators depended on whether prey species cooccurred, however, differed for each of the response variables. Predators affected snail body growth via nonconsumptive mechanisms, but the change in the overall effect of predators on snail body growth was attributable to how snails responded to competition in the absence of predators, rather than a change in how snails responded to the threat of predation. Predators did not affect tadpole body growth via nonconsumptive mechanisms, but the greater vulnerability of competitively superior prey (snails) to predators increased the strength of consumptive mechanisms (and hence the overall effect) through which predators affected tadpole growth. Predators affected tadpole morphology via nonconsumptive mechanisms, but the greater propensity for predators to kill competitively superior prey (snails) enhanced the ability of tadpoles to alter their morphology in response to the threat of predation by creating an environment where tadpoles had a higher per capita supply of food available to invest in the development of morphological defenses. Our work indicates that the mechanisms through which predators affect prey depends on the other members of the community.

Behavioral plasticity in response to perceived predation risk in breeding house wrens.

Predation is a significant cause of nest failure in passerine birds, and, thus, natural selection is expected to favor behavioral plasticity to allow birds to respond to perceived changes in predation risk. However, behavioral plasticity in response to perceived predation risk, and its potential fitness-related costs, are understudied. In a wild population of breeding house wrens (Troglodytes aedon), we tested the hypotheses that (1) birds show behavioral plasticity in response to perceived nest-predation risk to reduce self-risk or risk to offspring, but (2) this plasticity incurs fitness-related costs. We experimentally increased the perceived risk of nest predation by enlarging the diameter of the nestbox entrance from the standard 3.2 cm to 5.0 cm once incubation began. Unexpectedly, large-hole females spent significantly less time being vigilant than small-hole (control) females during late incubation. Both males and females also exhibited plasticity in their provisioning behavior. Large-hole males increased and large-hole females decreased provisioning visits with increasing brood size, whereas small-hole males and females behaved similarly and were unaffected by brood size. Females did not show plasticity in their incubation or brooding behavior. Notwithstanding this behavioral plasticity in response to increased perceived predation risk, treatment had no effect on hatching success or early hatchling survival, nor did it affect nestling body condition or fledging success. We conclude, therefore, that house wrens show behavioral plasticity in response to perceived nest-predation risk, but that any short-term fitness-related costs associated with this flexibility appear negligible.

Predator-induced delayed maturity in bluegill sunfish (Lepomis macrochirus): variation among populations.

Previous studies suggested that differences in age at maturity among populations of bluegill sunfish (Lepomis macrochirus) were not genetically based, but rather were a phenotypic response to the presence of predators. I conducted two experiments to determine if the presence of largemouth bass affected age at maturity in bluegill sunfish. Bluegills from three populations were tested to see if the response to the threat of predation varied among source populations. Juvenile bluegills were maintained in the presence of predators or in controls with no contact with predators. Refuge use and growth were monitored during the experiments and reproductive activity was evaluated when bluegills reached age 1. Bluegills from one population exhibited delayed maturity in the presence of predators. Individuals from the other two populations showed no significant differences between predator and control treatments. The population that responded to the presence of predators had a history of high predation levels over the past 30-40 years. The other populations had a history of low levels of predation. This study suggests that presence of predators can induce phenotypic shifts in age at maturity of bluegills, but that the magnitude of response varies among populations in a manner consistent with historical patterns of coexistence.