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.

Noise pollution alters the diet composition of invertebrate consumers both in and beyond a noise-exposed grassland ecosystem.

Anthropogenic noise is ubiquitous globally. However, we know little about how the impacts of noise alter fundamental ecosystem properties, such as resource consumption by invertebrate consumers. Using experimental noise manipulation and faecal DNA metabarcoding, we assessed how the direct and cross-trophic indirect effects of noise altered the dietary richness and specializations of omnivorous grasshoppers in a grassland ecosystem. We found that the experimental noise treatment expanded grasshoppers' dietary richness and resulted in dietary generalizations in both noise-exposed and adjacent relatively quieter areas. Unexpectedly, however, these dietary changes were primarily explained by the direct effect of noise not only in the noise-exposed areas but also in the adjacent quieter areas and were relaxed by indirect effects of noise such as reduced birds and predation risk and increased grasshoppers. Our work suggests that noise pollution can be key in explaining the variation of invertebrate consumers' diets across a gradient of noise-exposed environments.

Avian Predators Avoid Attacking Fly-Mimicking Beetles: A Field Experiment on Evasive Mimicry Using Artificial Prey.

AbstractMany Neotropical beetles present coloration patterns mimicking red-eyed flies, which are presumably evasive mimicry models. However, the role of predators in selecting for evasive mimics in nature remains untested. In a field experiment, we used nontoxic plasticine replicas of a specialized fly-mimicking beetle species, which we placed on the host plants of the beetles. We show that replicas painted with reddish patches simulating the eyes of flesh flies experienced a much lower predation rate than control replicas. We found that beak marks were the most frequent signs of attack on plasticine replicas, underlining the potential selective pressure exerted by birds. Replicas that matched the size of the beetles suffered higher predation than smaller or larger replicas. The predation rate was also higher for beetle replicas exposed during the warm and wet season, when adult beetles occur. Our results support predator-mediated selection of mimic beetles, highlighting that reddish spots resembling flies' eyes comprise an important trait in reducing attack by avian predators.

Local adaptation in trait-mediated trophic cascades.

Predator-induced changes in prey foraging can influence community dynamics by increasing the abundance of basal resources via a trait-mediated trophic cascade. The strength of these cascades may be altered by eco-evolutionary relationships between predators and prey, but the role of basal resources has received limited attention. We hypothesized that trait-mediated trophic cascade strength may be shaped by selection from trophic levels above and below prey. Field and laboratory experiments used snails (Nucella lapillus) from two regions in the Gulf of Maine (GoM) that vary in basal resource availability (e.g. mussels), seawater temperature, and contact history with the invasive green crab, Carcinus maenas. In field and laboratory experiments, Nucella from both regions foraged on mussels in the presence or absence of green crab risk cues. In the field, Nucella from the northern GoM, where mussels are scarce, were less responsive to risk cues and more responsive to seawater temperature than southern Nucella. In the lab, however, northern Nucella foraged and grew more than southern snails in the presence of risk, but foraging and growth were similar in the absence of risk. We suggest that adaptation to basal resource availability may shape geographical variation in the strength of trait-mediated trophic cascades.

Behavioural responses to mammalian grazing expose insect herbivores to elevated risk of avian predation.

Large mammalian herbivores (LMH) are important functional components and drivers of biodiversity and ecosystem functioning in grasslands. Yet their role in regulating food-web dynamics and trophic cascades remains poorly understood. In the temperate grasslands of northern China, we explored whether and how grazing domestic cattle (Bos taurus) alter the predator-prey interactions between a dominant grasshopper (Euchorthippus unicolor) and its avian predator the barn swallow (Hirundo rustica). Using two large manipulative field experiments, we found that in the presence of cattle, grasshoppers increased their jumping frequency threefold, swallows increased foraging visits to these fields sixfold, and grasshopper density was reduced by about 50%. By manipulatively controlling the grasshoppers' ability to jump, we showed that jumping enables grasshoppers to avoid being incidentally consumed or trampled by cattle. However, jumping behaviour increased their consumption rates by swallows 37-fold compared with grasshoppers that were unable to jump. Our findings illustrate how LMH can indirectly alter predator-prey interactions by affecting behaviour of avian predators and herbivorous insects. These non-plant-mediated effects of LMH may influence trophic interactions in other grazing ecosystems and shape community structure and dynamics. We highlight that convoluted multispecies interactions may better explain how LMH control food-web dynamics in grasslands.

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.

Sensory cues of predation risk generate sex-specific changes in neural activity and behavior, but not hormones, in Trinidadian guppies.

How an organism responds to risk depends on how that individual perceives such risk. Integrating cues from multiple sensory modalities allows individuals to extract information from their environment, and whether and how the brain and body respond differently to different sensory cues can help reveal mechanistic decision-making processes. Here, we assessed neural, hormonal, and behavioral responses to different sensory cues of predation risk in Trinidadian guppies (Poecilia reticulata). Adult guppies were assigned to one of four treatment groups: control, visual, olfactory, and both sensory cues combined from a natural predator, the pike cichlid (Crenicichla alta), for 2 h. We found no difference in glucocorticoid response to any cue. However, we found behavioral and neural activation responses to olfactory-only cues. In addition, we found a sex by treatment effect, where males showed greater changes in neural activation in brain regions associated with avoidance behavior, while females showed greater changes in neural activation in regions associated with social behavior and memory, mirroring sex by treatment differences in behavioral antipredator responses. Altogether, our results demonstrate that single and combinatory cues may influence risk-taking behavior differently based on sex, suggesting that perception and integration of cues can cascade into sex differences in behavior.

Do domestic budgerigars perceive predation risk?

Predation risk may affect the foraging behavior of birds. However, there has been little research on the ability of domestic birds to perceive predation risk and thus adjust their feeding behavior. In this study, we tested whether domestic budgerigars (Melopsittacus undulatus) perceived predation risk after the presentation of specimens and sounds of sparrowhawks (Accipiter nisus), domestic cats (Felis catus), and humans, and whether this in turn influenced their feeding behavior. When exposed to visual or acoustic stimuli, budgerigars showed significantly longer latency to feed under sparrowhawk, domestic cat, and human treatments than with controls. Budgerigars responded more strongly to acoustic stimuli than visual stimuli, and they showed the longest latency to feed and the least number of feeding times in response to sparrowhawk calls. Moreover, budgerigars showed shorter latency to feed and greater numbers of feeding times in response to human voices than to sparrowhawk or domestic cat calls. Our results suggest that domestic budgerigars may identify predation risk through visual or acoustic signals and adjust their feeding behavior accordingly.

Predation risk drives long-term shifts in migratory behaviour and demography in a large herbivore population.

Migration is an adaptive life-history strategy across taxa that helps individuals maximise fitness by obtaining forage and avoiding predation risk. The mechanisms driving migratory changes are poorly understood, and links between migratory behaviour, space use, and demographic consequences are rare. Here, we use a nearly 20-year record of individual-based monitoring of a large herbivore, elk (Cervus canadensis) to test hypotheses for changing patterns of migration in and adjacent to a large protected area in Banff National Park (BNP), Canada. We test whether bottom-up (forage quality) or top-down (predation risk) factors explained trends in (i) the proportion of individuals using 5 different migratory tactics, (ii) differences in survival rates of migratory tactics during migration and whilst on summer ranges, (iii) cause-specific mortality by wolves and grizzly bears, and (iv) population abundance. We found dramatic shifts in migration consistent with behavioural plasticity in individual choice of annual migratory routes. Shifts were inconsistent with exposure to the bottom-up benefits of migration. Instead, exposure to landscape gradients in predation risk caused by exploitation outside the protected area drove migratory shifts. Carnivore exploitation outside the protected area led to higher survival rates for female elk remaining resident or migrating outside the protected area. Cause-specific mortality aligned with exposure to predation risk along migratory routes and summer ranges. Wolf predation risk was higher on migratory routes than summer ranges of montane-migrant tactics, but wolf predation risk traded-off with heightened risk from grizzly bears on summer ranges. A novel eastern migrant tactic emerged following a large forest fire that enhanced forage in an area with lower predation risk outside of the protected area. The changes in migratory behaviour translated to population abundance, where abundance of the montane-migratory tactics declined over time. The presence of diverse migratory life histories maintained a higher total population abundance than would have been the case with only one migratory tactic in the population. Our study demonstrates the complex ways in which migratory populations change over time through behavioural plasticity and associated demographic consequences because of individuals balancing predation risk and forage trade-offs.

Food-safety trade-offs drive dynamic behavioural antipredator responses among snowshoe hares.

Prey adopt various antipredator responses to minimize the risk of predation, and the fitness costs of antipredator responses can have emergent effects on the population dynamics of prey species. While the trade-off between food acquisition and predation avoidance has long been recognized in predicting antipredator responses, less attention has been paid to the dynamics of the food-safety trade-off driven by temporal variation in multiple risk factors under changing seasonal conditions. Here, we monitored foraging and vigilance behaviour of a central prey species, snowshoe hares (Lepus americanus), at fine temporal scales over the winter with various types of predation risk, while also experimentally manipulating predation risk by attracting predators to foraging patches. Hares increased foraging and decreased vigilance over the winter, but hares under chronic risk decreased their antipredator efforts to a lesser degree, indicating that those individuals prioritized risk avoidance over food acquisition. Hares also decreased foraging and increased antipredator efforts in response to the temporal activity of predators and environmental cues of predation risk. However, the magnitude of the responses to the environmental cues was mediated by time of winter. While we did not detect a reactive response of hares to acute risk, we did find that hares exhibiting camouflage mismatch proactively increased vigilance. Overall, our results highlight the importance of species-specific traits and changing seasonal conditions in addition to temporal variation in multiple risk factors in predicting antipredator responses and the context dependence of risk effects.

The transgenerational consequences of paternal social isolation and predation exposure in threespined sticklebacks.

Parents routinely encounter stress in the ecological environment that can affect offspring development (transgenerational plasticity: TGP); however, parents' interactions with conspecifics may alter how parents respond to ecological stressors. During social buffering, the presence of conspecifics can reduce the response to or increase the speed of recovery from a stressor. This may have cascading effects on offspring if conspecifics can mitigate parental responses to ecological stress in ways that blunt the transmission of stress-induced transgenerational effects. Here, we simultaneously manipulated both paternal social isolation and experience with predation risk prior to fertilisation in threespined stickleback (Gasterosteus aculeatus). We generated offspring via in-vitro fertilisation to allow us to isolate paternal effects mediated via sperm alone (i.e. in the absence of paternal care). If social buffering mitigates TGP induced by paternal exposure to predation risk, then we expect the transgenerational effects of predation exposure to be weaker when a conspecific is present compared to when the father is isolated. Offspring of predator-exposed fathers showed reduced anxiety-like behaviour and tended to be captured faster by the predator. Fathers who were socially isolated also had offspring that were captured faster by a live predator, suggesting that paternal social isolation may have maladaptive effects on how offspring respond to ecological stressors. Despite additive effects of paternal social isolation and paternal predation risk, we found no evidence of an interaction between these paternal treatments, suggesting that the presence of a conspecific did not buffer fathers and/or offspring from the effects of predation risk. Our results suggest that socially induced stress is an important, yet underappreciated, mediator of TGP and can elicit transgenerational effects even in species that do not form permanent social groups. Future studies should therefore consider how the parental social environment can affect both within and trans-generational responses to ecological stressors.

Size dependent antipredator responses in a fish-shrimp mutualism.

For prey, taking refuge from predators has obvious fitness benefits but may also be costly by impinging on time and effort available for feeding or attracting mates. The antipredator responses of refuge-seeking animals are therefore predicted to vary strategically depending on how threatening they perceive the risk. To test this, we studied the impacts of a simulated predatory threat on the antipredator responses of wild sandy prawn-gobies (Ctenogobiops feroculus) that co-inhabit burrows with Alpheus shrimp (family Alpheidae) in a mutualistic relationship. We exposed goby-shrimp pairs, repeatedly on three separate occasions, to an approaching threat and measured the antipredator behaviours of both partners. We found that re-emerging from the burrow took longer in large compared to small fish. Moreover, quicker re-emergence by small-but not medium or large-sized gobies-was associated with an earlier flight from the approaching threat (i.e. when the threat was still further away). Finally, the goby and shrimp sharing a burrow were matched in body size and their risk-taking behaviour was highly dependent on one another. The findings contribute to our understanding of how an individual's phenotype and perception of danger relates to its risk-taking strategy, and how mutualistic partners can have similar risk sensitivities.

Parenting in a changing environment: A long-term study of prolactin, parental effort and reproductive success in common eiders.

Parental care is regulated by multiple endocrine mechanisms. Among these hormones, prolactin (PRL) is involved in the expression of parental behaviors. Despite the consensus that PRL mediates variation in parental effort with age and body condition, its role in the adjustment of parental effort to fluctuating environmental conditions, including changing predation pressure, still awaits further investigation. To shed light on this knowledge gap, we relied on a long-term monitoring of female common eiders Somateria mollissima (n = 1277 breeding attempts, 2012-2022) incubating under fluctuating predation risk to investigate the link between baseline PRL levels and female minimum age, body condition, clutch size, environmental parameters (predation pressure, climate, nest microhabitat) and hatching success. We predicted that PRL would be higher in older females, those in better condition or incubating larger clutches. We also predicted that females would reduce parental effort when nesting under challenging environmental conditions (high predation pressure or poor climatic conditions), translated into reduced baseline PRL levels. We also explored how variation in PRL levels, female characteristics and environmental parameters were related to hatching success. Following our predictions, PRL levels were positively associated with body condition and female age (before showing a senescent decline in the oldest breeders). However, we did not observe any population-level or individual-level reduction in PRL levels in response to increasing predation pressure. Population-level baseline PRL levels instead increased over the study period, coincident with rising predation threat, but also increasing female body condition and age. While we did not provide evidence for a direct association between baseline PRL levels and predation risk, our results support the idea that elevated baseline PRL levels promote hatching success under internal constraints (in young, inexperienced, breeders or those incubating a large clutch) or constraining environmental conditions (during years of high predation pressure or poor climatic and foraging conditions). Finally, the low repeatability of baseline PRL levels and high interannual variability highlight considerable within-individual flexibility in baseline PRL levels. Further research should explore flexibility in parental effort to changing environmental conditions, focusing on both baseline and stress-induced PRL levels.

Foraging trade-offs, flagellar arrangements, and flow architecture of planktonic protists.

Unicellular flagellated protists are a key element in aquatic microbial food webs. They all use flagella to swim and to generate feeding currents to encounter prey and enhance nutrient uptake. At the same time, the beating flagella create flow disturbances that attract flow-sensing predators. Protists have highly diverse flagellar arrangements in terms of number of flagella and their position, beat pattern, and kinematics, but it is unclear how the various arrangements optimize the fundamental trade-off between resource acquisition and predation risk. Here we describe the near-cell flow fields produced by 15 species and demonstrate consistent relationships between flagellar arrangement and swimming speed and between flagellar arrangement and flow architecture, and a trade-off between resource acquisition and predation risk. The flow fields fall in categories that are qualitatively described by simple point force models that include the drag force of the moving cell body and the propulsive forces of the flagella. The trade-off between resource acquisition and predation risk varies characteristically between flow architectures: Flagellates with multiple flagella have higher predation risk relative to their clearance rate compared to species with only one active flagellum, with the exception of the highly successful dinoflagellates that have simultaneously achieved high clearance rates and stealth behavior due to a unique flagellar arrangement. Microbial communities are shaped by trade-offs and environmental constraints, and a mechanistic explanation of foraging trade-offs is a vital part of understanding the eukaryotic communities that form the basis of pelagic food webs.

Density-dependent habitat selection alters drivers of population distribution in northern Yellowstone elk.

Although it is well established that density dependence drives changes in organismal abundance over time, relatively little is known about how density dependence affects variation in abundance over space. We tested the hypothesis that spatial trade-offs between food and safety can change the drivers of population distribution, caused by opposing patterns of density-dependent habitat selection (DDHS) that are predicted by the multidimensional ideal free distribution. We addressed this using winter aerial survey data of northern Yellowstone elk (Cervus canadensis) spanning four decades. Supporting our hypothesis, we found positive DDHS for food (herbaceous biomass) and negative DDHS for safety (openness and roughness), such that the primary driver of habitat selection switched from food to safety as elk density decreased from 9.3 to 2.0 elk/km2 . Our results demonstrate how population density can drive landscape-level shifts in population distribution, confounding habitat selection inference and prediction and potentially affecting community-level interactions.

Riskiness of Movement Lifestyle Varies Inversely with Adult Survival Probability among Species.

AbstractWhy do species differ in their movement lifestyles? Animals that spend more time sitting motionless and acquire food using less conspicuous movements can be more vigilant and less obvious to predators. More active animals that use food types and sites that require more conspicuous behaviors increase vulnerability to predators. Life history theory predicts that aversiveness to mortality risk evolves inversely to adult survival probability. Consequently, we postulated that long-lived species evolved inconspicuous movement lifestyles, whereas shorter-lived species use more conspicuous movement lifestyles. We tested this hypothesis by quantifying the movement lifestyles of nine tropical songbird species. Use of conspicuous movement and foraging behaviors, such as flying and hovering, was greatest in shorter-lived species and decreased with increasing adult survival probability across species. Similarly, foraging speed decreased with increasing adult survival based on a meta-analysis of 64 songbird species. Faster and conspicuous movement lifestyles of shorter-lived species likely increase food acquisition rates, which fits with faster life history strategies that include more feeding trips for young and faster growth. Similarly, slow movement lifestyles of long-lived species fit with the reduced food needs of slower life history strategies. Movement lifestyles may have evolved as an integrated component of the slow-fast life history continuum.

Sensory integration of danger and safety cues may explain the fear of a quiet coyote.

Sensory integration theory predicts natural selection should favour adaptive responses of animals to multiple forms of information, yet empirical tests of this prediction are rare, particularly in free-living mammals. Studying indirect predator cues offers a salient opportunity to inquire about multimodal risk assessment and its potentially interactive effects on prey responses. Here we exposed California ground squirrels from two study sites (that differ in human and domestic dog activity) to acoustic and/or olfactory predator cues to reveal divergent patterns of signal dominance. Olfactory information most strongly predicted space use within the testing arena. That is, individuals, especially those at the human-impacted site, avoided coyote urine, a danger cue that may communicate the proximity of a coyote. By contrast, subjects allocated less time to risk-sensitive behaviours when exposed to acoustic cues. Specifically, although individuals were consistent in their behavioural responses across trials, 'quiet coyotes' (urine without calls) significantly increased the behavioural reactivity of prey, likely because coyotes rarely vocalize when hunting. More broadly, our findings highlight the need to consider the evolution of integrated fear responses and contribute to an emerging understanding of how animals integrate multiple forms of information to trade off between danger and safety cues in a changing world.

When death comes: linking predator-prey activity patterns to timing of mortality to understand predation risk.

The assumption that activity and foraging are risky for prey underlies many predator-prey theories and has led to the use of predator-prey activity overlap as a proxy of predation risk. However, the simultaneous measures of prey and predator activity along with timing of predation required to test this assumption have not been available. Here, we used accelerometry data on snowshoe hares (Lepus americanus) and Canada lynx (Lynx canadensis) to determine activity patterns of prey and predators and match these to precise timing of predation. Surprisingly we found that lynx kills of hares were as likely to occur during the day when hares were inactive as at night when hares were active. We also found that activity rates of hares were not related to the chance of predation at daily and weekly scales, whereas lynx activity rates positively affected the diel pattern of lynx predation on hares and their weekly kill rates of hares. Our findings suggest that predator-prey diel activity overlap may not always be a good proxy of predation risk, and highlight a need for examining the link between predation and spatio-temporal behaviour of predator and prey to improve our understanding of how predator-prey behavioural interactions drive predation risk.

Individual response in body mass and basal metabolism to the risks of predation and starvation in passerines.

Wintering energy management in small passerines has focused on the adaptive regulation of the daily acquisition of energy reserves within a starvation-predation trade-off framework. However, the possibility that the energetic cost of living, i.e. basal metabolic rate (BMR), is being modulated as part of the management energy strategy has been largely neglected. Here, we addressed this possibility by experimentally exposing captive great tits (Parus major) during winter to two consecutive treatments of increased starvation and predation risk for each individual bird. Body mass and BMR were measured prior to and after each week-long treatment. We predicted that birds should be lighter but with a higher metabolic capacity (higher BMR) as a response to increased predation risk, and that birds should increase internal reserves while reducing their cost of living (lower BMR) when exposed to increased starvation risk. Wintering great tits kept a constant body mass independently of a week-long predation or starvation treatment. However, great tits reduced the cost of living (lower BMR) when exposed to the starvation treatment, while BMR remained unaffected by the predation treatment. Energy management in wintering small birds partly relies on BMR regulation, which challenges the current theoretical framework based on body mass regulation.

Predation stress experienced as immature mites extends their lifespan.

The early-life experience is important in modulating the late-life performance of individuals. It has been predicted that there were trade-offs between early-life fitness and late-life success. Most of the studies on senescence have focused on the trade-offs between the reproduction and lifespan, and the influences of diet, mating, and other factors. Because the negative, non-consumptive effects of predators could also modulate the behaviour and underlying mechanisms of the prey, this study aimed to examine the different effects of predator-induced stress experienced in the early life compared with later life of the prey. The prey (Tyrophagus putrescentiae) was exposed to predation stress from the predator (Neoseiulus cucumeris) during different periods of its life (immature, oviposition period, and post-oviposition period). The results showed that the predation stress experienced during immature stages delayed development by 7.3% and prolonged lifespan by 9.7%, while predation stress experienced in the adult stage (both oviposition and post-oviposition periods) decreased lifespans of T. putrescentiae (by 24.8% and 28.7%, respectively). Predation stress experienced during immature stages also reduced female fecundity by 7.3%, whereas that experienced during the oviposition period reduced fecundity of the prey by 50.7%. This study demonstrated for the first time lifespan extension by exposure to predation stress when young and highlighted the importance of early-life experience to aging and lifespan.