Fear of predators in free-living wildlife reduces population growth over generations.

Correctly assessing the total impact of predators on prey population growth rates (lambda, λ) is critical to comprehending the importance of predators in species conservation and wildlife management. Experiments over the past decade have demonstrated that the fear (antipredator responses) predators inspire can affect prey fecundity and early offspring survival in free-living wildlife, but recent reviews have highlighted the absence of evidence experimentally linking such effects to significant impacts on prey population growth. We experimentally manipulated fear in free-living wild songbird populations over three annual breeding seasons by intermittently broadcasting playbacks of either predator or nonpredator vocalizations and comprehensively quantified the effects on all the components of population growth, together with evidence of a transgenerational impact on offspring survival as adults. Fear itself significantly reduced the population growth rate (predator playback mean λ = 0.91, 95% CI = 0.80 to 1.04; nonpredator mean λ = 1.06, 95% CI = 0.96 to 1.16) by causing cumulative, compounding adverse effects on fecundity and every component of offspring survival, resulting in predator playback parents producing 53% fewer recruits to the adult breeding population. Fear itself was consequently projected to halve the population size in just 5 years, or just 4 years when the evidence of a transgenerational impact was additionally considered (λ = 0.85). Our results not only demonstrate that fear itself can significantly impact prey population growth rates in free-living wildlife, comparing them with those from hundreds of predator manipulation experiments indicates that fear may constitute a very considerable part of the total impact of predators.

Fear of the human 'super predator' in native marsupials and introduced deer in Australia.

Recent experiments have demonstrated that carnivores and ungulates in Africa, Asia, Europe and North America fear the human 'super predator' far more than other predators. Australian mammals have been a focus of research on predator naiveté because it is suspected they show atypical antipredator responses. To experimentally test if mammals in Australia also most fear humans, we quantified the responses of four native marsupials (eastern grey kangaroo, Bennett's wallaby, Tasmanian pademelon, common brushtail possum) and introduced fallow deer to playbacks of predator (human, dog, Tasmanian devil, wolf) or non-predator control (sheep) vocalizations. Native marsupials most feared the human 'super predator', fleeing humans 2.4 times more often than the next most frightening predator (dogs), and being most, and significantly, vigilant to humans. These results demonstrate that native marsupials are not naïve to the peril humans pose, substantially expanding the taxonomic and geographic scope of the growing experimental evidence that wildlife worldwide generally perceive humans as the planet's most frightening predator. Introduced fallow deer fled humans, but not more than other predators, which we suggest may result from their being introduced. Our results point to both challenges concerning marsupial conservation and opportunities for exploiting fear of humans as a wildlife management tool.

Rain, recreation and risk: Human activity and ecological disturbance create seasonal risk landscapes for the prey of an ambush predator.

Predation risk and prey responses exhibit fluctuations in space and time. Seasonal ecological disturbances can alter landscape structure and permeability to influence predator activity and efficacy, creating predictable patterns of risk for prey (seasonal risk landscapes). This may create corresponding seasonal shifts in antipredator behaviour, mediated by species ecology and trade-offs between risk and resources. Yet, how human recreation interacts with seasonal risk landscapes and antipredator behaviour remains understudied. In South Florida, we investigated the impact of a seasonal ecological disturbance, specifically flooding, which is inversely related to human activity, on interactions between Florida panthers (Puma concolor coryi) and white-tailed deer (Odocoileus virginianus). We hypothesized that human activity and ecological disturbances would interact with panther-deer ecology, resulting in the emergence of two distinct seasonal landscapes of predation risk and the corresponding antipredator responses. We conducted camera trap surveys across southwestern Florida to collect detection data on humans, panthers and deer. We analysed the influence of human site use and flooding on deer and panther detection probability, co-occurrence and diel activity during the flooded and dry seasons. Flooding led to decreased panther detections and increased deer detections, resulting in reduced deer-panther co-occurrence during the flooded season. Panthers exhibited increased nocturnality and reduced diel activity overlap with deer in areas with higher human activity. Supporting our hypothesis, panthers' avoidance of human recreation and flooding created distinct risk schedules for deer, driving their antipredator behaviour. Deer utilized flooded areas to spatially offset predation risk during the flooded season while increasing diurnal activity in response to human recreation during the dry season. We highlight the importance of understanding how competing risks and ecological disturbances influence predator and prey behaviour, leading to the generation of seasonal risk landscapes and antipredator responses. We emphasize the role of cyclical ecological disturbances in shaping dynamic predator-prey interactions. Furthermore, we highlight how human recreation may function as a 'temporal human shield,' altering seasonal risk landscapes and antipredator responses to reduce encounter rates between predators and prey.

Prey tells, large herbivores fear the human 'super predator'.

Fear of the human 'super predator' has been demonstrated to so alter the feeding behavior of large carnivores as to cause trophic cascades. It has yet to be experimentally tested if fear of humans has comparably large effects on the feeding behavior of large herbivores. We conducted a predator playback experiment exposing white-tailed deer to the vocalizations of humans, extant or locally extirpated non-human predators (coyotes, cougars, dogs, wolves), or non-predator controls (birds), at supplemental food patches to measure the relative impacts on deer feeding behavior. Deer were more than twice as likely to flee upon hearing humans than other predators, and hearing humans was matched only by hearing wolves in reducing overall feeding time gaged by visits to the food patch in the following hour. Combined with previous, site-specific research linking deer fecundity to predator abundance, this study reveals that fear of humans has the potential to induce a larger effect on ungulate reproduction than has ever been reported. By demonstrating that deer most fear the human 'super predator', our results point to the fear humans induce in large ungulates having population- and community-level impacts comparable to those caused by the fear humans induce in large carnivores.

The role of hunting on Sapajus xanthosternos' landscape of fear in the Atlantic Forest, Brazil.

Habitats with spatial variation in food availability, predation risk, and hunting pressure allow us to study how animals resolve the trade-off between food searching and predator avoidance. We investigated the influence of food availability, predation risk, and the perceived predation risk on habitat use by a primate living under high hunting pressure, the yellow-breasted capuchin monkeys, Sapajus xanthosternos, at Una Biological Reserve (ReBio Una). We hypothesized that the hunting pressure occurring in the capuchins' home range would favor predator avoidance to the detriment of searching for food. We characterized a set of covariates related to resource availability (fruit and invertebrate biomasses, feeding on dispersed and clumped food items, sleeping sites), perceived predation risk (alarm calls given to terrestrial and aerial predators, silent group movement, and vigilance behavior), and actual predation risk (evidence of hunting) and estimated their effects on how one group of capuchin monkeys uses its habitat. The group divides its time among three major forest types within their home range: agroforest, mature, and secondary. Our results suggest that the actual and perceived risk of hunting by humans, as well as the perceived predation risk by both terrestrial and aerial predators, were significant determinants of capuchin monkeys' space use. Yellow-breasted capuchin monkeys' space use was negatively related to the risk of hunting by humans (actual evidence and silent behavior), the perceived risk of predation by both aerial and terrestrial predators, and the presence of sleeping sites. Capuchin monkeys' use of space was not related to the biomass of fruits in the habitat, and the biomass of invertebrates had a very low positive effect. We confirmed our prediction that in a habitat with high hunting pressure, the risk of predation, both perceived and actual, had a more significant impact on how yellow-breasted capuchins used space than did food availability.

Chronic anthropogenic noise disrupts glucocorticoid signaling and has multiple effects on fitness in an avian community.

Anthropogenic noise is a pervasive pollutant that decreases environmental quality by disrupting a suite of behaviors vital to perception and communication. However, even within populations of noise-sensitive species, individuals still select breeding sites located within areas exposed to high noise levels, with largely unknown physiological and fitness consequences. We use a study system in the natural gas fields of northern New Mexico to test the prediction that exposure to noise causes glucocorticoid-signaling dysfunction and decreases fitness in a community of secondary cavity-nesting birds. In accordance with these predictions, and across all species, we find strong support for noise exposure decreasing baseline corticosterone in adults and nestlings and, conversely, increasing acute stressor-induced corticosterone in nestlings. We also document fitness consequences with increased noise in the form of reduced hatching success in the western bluebird (Sialia mexicana), the species most likely to nest in noisiest environments. Nestlings of all three species exhibited accelerated growth of both feathers and body size at intermediate noise amplitudes compared with lower or higher amplitudes. Our results are consistent with recent experimental laboratory studies and show that noise functions as a chronic, inescapable stressor. Anthropogenic noise likely impairs environmental risk perception by species relying on acoustic cues and ultimately leads to impacts on fitness. Our work, when taken together with recent efforts to document noise across the landscape, implies potential widespread, noise-induced chronic stress coupled with reduced fitness for many species reliant on acoustic cues.

Pathogen vs. predator: ranavirus exposure dampens tadpole responses to perceived predation risk.

There is increasing interest in how animals respond to multiple stressors, including potential synergistic or antagonistic interaction between pathogens and perceived predation risk (PPR). For prey that exhibit phenotypic plasticity, it is unclear whether infection and PPR affect behaviour and morphology independently, or in an antagonistic or synergistic manner. Using a 2 × 2 factorial experiment involving green frog (Lithobates clamitans) tadpoles exposed to ranavirus (FV3) and larval dragonflies (Anax spp.), we assessed whether anti-predator responses were affected by infection. We found that activity and feeding were reduced additively by both stressors. Body mass of tadpoles from FV3-exposed tanks was lighter relative to control and PPR-only tanks, while metabolism was comparable across treatments. We found that FV3 exposure compromised morphometric responses to PPR in an antagonistic manner: tadpoles exposed to both treatments had restricted changes in tail depth compared to those receiving singular treatment. We conclude that multiple stressors can have complex and substantive effects on organisms, and that interactions between stressors may yield a range of responses depending on the level of exposure and sensitivity of the organism. Additional work should more fully determine mechanisms underlying the complex interplay between infection and predation risk, across a range of environmental conditions.

Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography.

Fear itself (perceived predation risk) can affect wildlife demography, but the cumulative impact of fear on population dynamics is not well understood. Parental care is arguably what most distinguishes birds and mammals from other taxa, yet only one experiment on wildlife has tested fear effects on parental food provisioning and the repercussions this has for the survival of dependent offspring, and only during early-stage care. We tested the effect of fear on late-stage parental care of mobile dependent offspring, by locating radio-tagged Song Sparrow fledglings and broadcasting predator or non-predator playbacks in their vicinity, measuring their parent's behavior and their own, and tracking the offspring's survival to independence. Fear significantly reduced late-stage parental care, and parental fearfulness (as indexed by their reduction in provisioning when hearing predators) significantly predicted their offspring's condition and survival. Combining results from this experiment with that on early-stage care, we project that fear itself is powerful enough to reduce late-stage survival by 24%, and cumulatively reduce the number of young reaching independence by more than half, 53%. Experiments in invertebrate and aquatic systems demonstrate that fear is commonly as important as direct killing in affecting prey demography, and we suggest focusing more on fear effects and on offspring survival will reveal the same for wildlife.

A phantom road experiment reveals traffic noise is an invisible source of habitat degradation.

Decades of research demonstrate that roads impact wildlife and suggest traffic noise as a primary cause of population declines near roads. We created a "phantom road" using an array of speakers to apply traffic noise to a roadless landscape, directly testing the effect of noise alone on an entire songbird community during autumn migration. Thirty-one percent of the bird community avoided the phantom road. For individuals that stayed despite the noise, overall body condition decreased by a full SD and some species showed a change in ability to gain body condition when exposed to traffic noise during migratory stopover. We conducted complementary laboratory experiments that implicate foraging-vigilance behavior as one mechanism driving this pattern. Our results suggest that noise degrades habitat that is otherwise suitable, and that the presence of a species does not indicate the absence of an impact.

So many choices, so little time: Food preference and movement vary with the landscape of fear.

Spatial and temporal variation in perceived predation risk is an important determinant of movement and foraging activity of animals. Foraging in this landscape of fear, individuals need to decide where and when to move, and what resources to choose. Foraging theory predicts the outcome of these decisions based on energetic trade-offs, but complex interactions between perceived predation risk and preferences of foragers for certain functional traits of their resources are rarely considered. Here, we studied the interactive effects of perceived predation risk on food trait preferences and foraging behavior in bank voles (Myodes glareolus) in experimental landscapes. Individuals (n = 19) were subjected for periods of 24 h to two extreme, risk-uniform landscapes (either risky or safe), containing 25 discrete food patches, filled with seeds of four plant species in even amounts. Seeds varied in functional traits: size, nutrients, and shape. We evaluated whether and how risk modifies forager preference for functional traits. We also investigated whether perceived risk and distance from shelter affected giving-up density (GUD), time in patches, and number of patch visits. In safe landscapes, individuals increased time spent in patches, lowered GUD and visited distant patches more often compared to risky landscapes. Individuals preferred bigger seeds independent of risk, but in the safe treatment they preferred fat-rich over carb-rich seeds. Thus, higher densities of resource levels remained in risky landscapes, while in safe landscapes resource density was lower and less diverse due to selective foraging. Our results suggest that the interaction of perceived risk and dietary preference adds an additional layer to the cascading effects of a landscape of fear which affects biodiversity at resource level.

Forager-mediated cascading effects on food resource species diversity.

Perceived predation risk varies in space and time. Foraging in this landscape of fear alters forager-resource interactions via cascading nonconsumptive effects. Estimating these indirect effects is difficult in natural systems. Here, we applied a novel measure to quantify the diversity at giving-up density that allows to test how spatial variation in perceived predation risk modifies the diversity of multispecies resources at local and regional spatial levels. Furthermore, we evaluated whether the nonconsumptive effects on resource species diversity can be explained by the preferences of foragers for specific functional traits and by the forager species richness. We exposed rodents of a natural community to artificial food patches, each containing an initial multispecies resource community of eight species (10 items each) mixed in sand. We sampled 35 landscapes, each containing seven patches in a spatial array, to disentangle effects at local (patch) and landscape levels. We used vegetation height as a proxy for perceived predation risk. After a period of three nights, we counted how many and which resource species were left in each patch to measure giving-up density and resource diversity at the local level (alpha diversity) and the regional level (gamma diversity and beta diversity). Furthermore, we used wildlife cameras to identify foragers and assess their species richness. With increasing vegetation height, i.e., decreasing perceived predation risk, giving-up density, and local alpha and regional gamma diversity decreased, and patches became less similar within a landscape (beta diversity increased). Foragers consumed more of the bigger and most caloric resources. The higher the forager species richness, the lower the giving-up density, and alpha and gamma diversity. Overall, spatial variation of perceived predation risk of foragers had measurable cascading effects on local and regional resource species biodiversity, independent of the forager species. Thus, nonconsumptive predation effects modify forager-resource interactions and might act as an equalizing mechanism for species coexistence.

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.