Mesopredator suppression by an apex predator alleviates the risk of predation perceived by small prey

Predators can impact their prey via consumptive effects that occur through direct killing, and via non-consumptive effects that arise when the behaviour and phenotypes of prey shift in response to the risk of predation. Although predators'' consumptive effects can have cascading population-level effects on species at lower trophic levels there is less evidence that predators'' non-consumptive effects propagate through ecosystems. Here we provide evidence that suppression of abundance and activity of a mesopredator (the feral cat) by an apex predator (the dingo) has positive effects on both abundance and foraging efficiency of a desert rodent. Then by manipulating predators'' access to food patches we further the idea that apex predators provide small prey with refuge from predation by showing that rodents increased their habitat breadth and use of ‘risky′ food patches where an apex predator was common but mesopredators rare. Our study suggests that apex predators'' suppressive effects on mesopredators extend to alleviate both mesopredators'' consumptive and non-consumptive effects on prey.     

Cats and dogs: A mesopredator navigating risk and reward provisioned by an apex predator

Successfully perceiving risk and reward is fundamental to the fitness of an animal, and can be achieved through a variety of perception tactics. For example, mesopredators may “directly” perceive risk by visually observing apex predators, or may “indirectly” perceive risk by observing habitats used by predators. Direct assessments should more accurately characterize the arrangement of risk and reward; however, indirect assessments are used more frequently in studies concerning the response of GPS‐marked animals to spatiotemporally variable sources of risk and reward. We investigated the response of a mesopredator to the presence of risk and reward created by an apex predator, where risk and reward likely vary in relative perceptibility (i.e., degree of being perceptible). First, we tested whether coyotes (Canis latrans) use direct or indirect assessments to navigate the presence of mountain lions (Puma concolor; risk) and kills made by mountain lions (reward) in an area where coyotes were a common prey item for mountain lions. Second, we assessed the behavioral response of coyotes to direct encounters with mountain lions. Third, we evaluated spatiotemporal use of carrion by coyotes at kills made by mountain lions. Indirect assessments generally outperformed direct assessments when integrating analyses into a unified framework; nevertheless, our ability to detect direct perception in navigating to mountain lion kills was likely restricted by scale and sampling limitations (e.g., collar fix rates, unsampled kill sites). Rather than responding to the risk of direct encounters with mountain lions, coyotes facilitated encounters by increasing their movement rate, and engaged in risky behavior by scavenging at mountain lion kills. Coyotes appear to mitigate risk by using indirect perception to avoid mountain lions. Our predator–predator interactions and insights are nuanced and counter to the conventional predator–prey systems that have generated much of the predation risk literature.     

Snail responses to cues produced by an invasive decapod predator

Abstract. Cues released by predators and injured prey often induce shifts in prey behavior that allow prey to evade predators, but also affect prey resource use. I investigated the effects of chemical and mechanical signals produced by injured snails (Physella gyrina) and predatory crayfish (Procambarus clarkii) on microdistributions of P. gyrina. In an initial experiment, I observed snail responses to the presence of a caged crayfish predator, to injured conspecifics, or to both. There were significant effects of time and the treatment × time interaction on the proportion of snails moving above the water line, with greater proportions of snails above the water line at night than during the day and with weak snail crawl‐out behavior being elicited by caged crayfish at night, but not during the day. In a second experiment, I examined snail microdistributions when exposed to crayfish confined to a small cage within each aquarium, crayfish confined to half of each aquarium, and crayfish ranging freely throughout each aquarium. Snails responded most strongly to free‐ranging crayfish by moving above the water line, but also demonstrated significant, but reduced, crawl‐out responses to crayfish confined to half of each aquarium; however, snails did not respond behaviorally to crayfish confined to small cages. In both experiments, there were marginally significant effects of unfed caged crayfish on the proportions of snail populations hiding under benthic shelters, with this response being the strongest at the start of the experiments but weak overall (with only 4–5% of P. gyrina responding in each experiment). These results indicate that cues (e.g., chemical or mechanical) produced by predators altered prey microdistributions, but that the exact prey responses (e.g., moving above the water line or into horizontal or benthic refugia) depended on the intensity and nature of cues.     

A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats

Apex predators can limit the abundance and behaviour of mesopredators, thereby reducing predation on smaller species. We know less about whether native apex predators are effective in suppressing invasive mesopredators, a major global driver of vertebrate extinctions. We use the severe disease‐induced decline of an apex predator, the Tasmanian devil, as a natural experiment to test whether devils limit abundance of invasive feral cats and in turn protect smaller native prey. Cat abundance was c. 58% higher where devils had declined, which in turn negatively affected a smaller native prey species. Devils had a stronger limiting effect on cats than on a native mesopredator, suggesting apex predators may have stronger suppressive effects on evolutionarily naive species than coevolved species. Our results highlight how disease in one species can affect the broader ecosystem. We show that apex predators not only regulate native species but can also confer resistance to the impacts of invasive populations. Apex predators could therefore be a powerful but underutilised tool to prevent biodiversity loss.     

Temporal variation in behavioral responses to dietary cues from a gape‐limited predator in tadpole prey: A test of the phylogenetic relatedness hypothesis

The ability of prey to recognize and adequately respond to predators determines their survival. Predator‐borne, post‐digestion dietary cues represent essential information for prey about the identity and the level of risk posed by predators. The phylogenetic relatedness hypothesis posits that prey should respond strongly to dietary cues from closely related heterospecifics but respond weakly to such cues from distantly related prey, following a hierarchical pattern. While such responses have mostly been observed in prey at their first encounter with predators, whether prey maintain such hierarchical levels of investment through time remains unclear. We investigated this question by exposing Rhacophorus arboreus tadpoles to the non‐consumptive effect of gape‐limited newt predators Cynops pyrrhogaster that were fed one of five prey diets across a gradient of phylogenetic relatedness: frog tadpoles (Rhacophorus arboreus, Rhacophorus schlegelii, Pelophylax nigromaculatus, and Hyla japonica) and medaka fish (Oryzias latipes). Predators’ diet, time, and their interaction significantly influenced tadpole activity level. We found support for the phylogenetic relatedness hypothesis: Investments in defense were stronger to cues from tadpole diets than to cues from fish diet. However, such a hierarchical response was recorded only in the first four days following predator exposure, then gradually disappear by day 8 on which the tadpoles exhibited similar activity level across all predator treatments. The findings suggest that, at least under the threat of gape‐limited predators, prey use phylogenetic information to evaluate risk and appropriately invest in defense during early encounters with predators; however, energy requirements may prevent prey from maintaining a high level of defense over long exposure to predation risk.     

Linking anti‐predator behaviour to prey demography reveals limited risk effects of an actively hunting large carnivore

Ecological theory predicts that the diffuse risk cues generated by wide‐ranging, active predators should induce prey behavioural responses but not major, population‐ or community‐level consequences. We evaluated the non‐consumptive effects (NCEs) of an active predator, the grey wolf (Canis lupus), by simultaneously tracking wolves and the behaviour, body fat, and pregnancy of elk (Cervus elaphus), their primary prey in the Greater Yellowstone Ecosystem. When wolves approached within 1 km, elk increased their rates of movement, displacement and vigilance. Even in high‐risk areas, however, these encounters occurred only once every 9 days. Ultimately, despite 20‐fold variation in the frequency of encounters between wolves and individual elk, the risk of predation was not associated with elk body fat or pregnancy. Our findings suggest that the ecological consequences of actively hunting large carnivores, such as the wolf, are more likely transmitted by consumptive effects on prey survival than NCEs on prey behaviour.     

Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey

Diet composition of a generalist predator, the red fox (Vulpes vulpes) in relation to season (winter or summer) and abundance of multi-annually cyclic voles was studied in western Finland from 1983 to 1995. The proportion of scats (PS; a total of 58 scats) including each food category was calculated for each prey group. Microtus voles (the field vole M. agrestis and the sibling vole M. rossiaemeridionalis) were the main prey group of foxes (PS = 0.55) and they frequently occurred in the scats both in the winter and summer (PSs 0.50 and 0.62, respectively). There was a positive correlation between the PSs of Microtus voles in the winter diet of foxes and the density indices of these voles in the previous autumn. Other microtine rodents (the bank vole Clethrionomys glareolus, the water vole Arvicola terrestris and the muskrat Ondatra zibethicus) were consumed more in winter than in summer. The unusually high small mustelid predation by red foxes (PS = approx. 0.10) in our study area gives qualitative support for the hypothesis on the limiting impact of mammalian predators on least weasel and stoat populations. None of the important prey groups was preyed upon more at low than at high densities of main prey (Microtus voles). This is consistent with the notion that red foxes are generalist predators that tend to opportunistically subsist on many prey groups. Among these prey groups, particularly hares and birds (including grouse), were frequently used as food by foxes.     

Generalization of learned predator recognition: an experimental test and framework for future studies

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.     

Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Responses of larval dragonflies to conspecific and heterospecific predator cues

Abstract.  1. In cannibalistic populations, smaller individuals are subject to predation by larger conspecifics, and small individuals commonly alter their behaviour in response to cannibals. Little is known, however, about the underlying cues that trigger such responses and how the behavioural responses to conspecific cannibals differ from heterospecific predators.
2. This study tests which cues are used for the detection of conspecific predators in the larva of the dragonfly Plathemis lydia and how the behavioural response to cannibals differed from the response to heterospecific predators.
3. Individuals were exposed to chemical cues, visual cues, and a combination of both cues from conspecifics as well as no predator and heterospecific predator controls during which their activity and feeding rates were observed.
4. Individuals increased their activity, spatial movement and feeding behaviour in response to either visual or chemical cues from conspecific predators, which was opposite to responses displayed with cues from heterospecific predators. Interestingly, the responses to visual and chemical cues from conspecifics combined were weaker than to either cue in isolation and similar to the no cue control.
5. The results clearly indicate that individuals are able to use chemical and visual cues to detect even very subtle differences in phenotype of conspecific predators.
6. The opposite response in behaviour when exposed to conspecific cannibals vs. heterospecific predators suggests that the presence of cannibals will increase the mortality risk of small individuals due to heterospecific predation. This risk-enhancement is likely to have important consequences for the dynamics of predator–prey interactions.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

Hypoxic refuges,predator–prey interactions and habitat selection by fishes

Localized hypoxic habitats were created in Delta Marsh, Manitoba, Canada to determine the potential of regions of moderate hypoxia to act as refuges for forage fishes from piscine predators. Minnow traps and giving‐up density (GUD) plates (plexiglas plates covered with trout crumble and fine gravel) were used to assess habitat use and perceived habitat quality for forage fishes, respectively, while passive integrated transponder tags provided data on habitat use by predator species to assess the level of predation risk. Data were collected both before and after a hypoxia manipulation (2–3 mg l^?1 dissolved oxygen, DO) to create a before–after control–effect style experiment. Fathead minnows Pimephales promelas were more abundant and consumed more food from GUD plates in hypoxic bays after the DO manipulation, indicating hypoxic locations were perceived as higher quality, lower‐risk habitats. The frequency of predator visits was not consistently affected. The duration of visits, and therefore the total time spent in these habitats, however, was significantly shorter. These predator data, combined with the prey information, are consistent with the hypothesis that hypoxic regions function as predator refuges. The refuge effect is not the result of predator exclusion, however; instead predators are rendered less capable of foraging and pose less of a threat in hypoxic locations.     

Behavioural responses of free‐ranging western grey kangaroos (Macropus fuliginosus) to olfactory cues of historical and recently introduced predators

Predation risk influences foraging decisions and time allocation of prey species, and may result in habitat shifts from potentially dangerous to safer areas. We examined a wild population of western grey kangaroos (Macropus fuliginosus) to test the efficacy of predator faecal odour in influencing time allocated to different behaviours and inducing changes in habitat use. Kangaroos were exposed to fresh faeces of a historical predator, the dingo (Canis lupus dingo), a recently introduced predator, the red fox (Vulpes vulpes), a herbivore (horse, Equus caballus) and an unscented control simultaneously. Kangaroos did not increase vigilance in predator‐scented areas. However, they investigated odour sources by approaching and sniffing; more time was spent investigating fox odour than control odours. Kangaroos then exhibited a clear anti‐predator response to predator odours, modifying their space use by rapidly escaping, then avoiding fox and dingo odour sources. Our results demonstrate that wild western grey kangaroos show behavioural responses to predator faeces, investigating then avoiding these olfactory cues of potential predation risk, rather than increasing general vigilance. This study contributes to our understanding of the impact of introduced mammalian predators on marsupial prey and demonstrates that a native Australian marsupial can recognize and respond to the odour of potential predators, including one that has been recently introduced.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species

Intraguild predation (IGP) has been increasingly recognized as an important interaction in ecological systems over the past two decades, and remarkable insights have been gained into its nature and prevalence. We have developed a technique using molecular gut-content analysis to compare the rate of IGP between closely related species of coccinellid beetles (lady beetles or ladybirds), which had been previously known to prey upon one another. We first developed PCR primers for each of four lady beetle species: Harmonia axyridis, Coccinella septempunctata, Coleomegilla maculata and Propylea quatuordecimpunctata. We next determined the prey DNA detection success over time (DS(50) ) for each combination of interacting species following a meal. We found that DS(50) values varied greatly between predator-prey combinations, ranging from 5.2 to 19.3 h. As a result, general patterns of detection times based upon predator or prey species alone are not discernable. We used the DS(50) values to correct field data to demonstrate the importance of compensation for detection times that are specific to particular predator-prey combinations.     

Not all predators are equal: a continent‐scale analysis of the effects of predator control on Australian mammals

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Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator,the Tasmanian devil

Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top–down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low.     

Both local presence and regional distribution of predator cues modulate prey colonisation in pond landscapes

Recent work on habitat selection has shown that the perceived quality of habitat patches may depend on the quality of adjacent patches. However, it is still unclear how local habitat selection cues can alter distribution patterns in metacommunities at a larger (regional) scale. We studied mosquito oviposition in pond landscapes that differed in the proportion of bad patches with fish predation risk. Our experiment provided conclusive evidence for two local and two regional types of habitat selection. Good patches near bad patches were avoided (local risk contagion) while more distant good patches experienced increased oviposition (regional compression). Oviposition in bad patches increased when located next to good patches (reward contagion) or when there were no good patches regionally present (regional compromise). This complex colonisation behaviour involving compromises at different spatial scales forces experimenters to reconsider the independence of spatial replicates and challenges available theories to predict species distribution patterns.