Seasonal differences in predation risk among seagrass epifauna species stabilize community\u2010level predation over time

Organisms that produce alternative, nondiscrete phenotypes in response to environmental conditions are expected to alter their phenotypes in relation to the degree of environmental change. This idea has been applied to the evolution of antipredator responses by prey, in which it has been hypothesized that prey should respond more strongly to predators that pose greater mortality risk. In a companion paper, I quantified predator-induced behavioral and morphological responses in six species of larval anurans across five different predator environments and found that these responses were prey- and predator-specific. In the present study, I addressed whether the responses were related to the level of predation risk posed by each of the predators. Within each prey species, I found that different predators posed different levels of predation risk; within each predator species, different prey species experienced different levels of risk. The differences in predation risk could be understood mechanistically after I quantified differences among predators in their ability to capture, handle, and consume prey and differences among prey in behavior and morphology. Using multivariate analyses, I found that predation risk had no significant effect on how a given prey responds to predators, although there were significant univariate behavioral effects; higher predation risk was related to greater decreases in activity and greater spatial avoidance. I also examined the relationship between risk and response across the six prey species within a predator treatment and found that higher predation risk across species leads to greater decreases in activity in the presence of Umbra and greater increases in tail depth in the presence of Anax. Thus, while previous studies have found relationships between predation risk and prey response when focusing on relatively few species, few predators, and a single trait, this more powerful test using 30 predator–prey combinations and nine traits suggests that the relationship is not well supported. This finding arises from the fact that larval anurans, as well as many other taxa, exhibit predator- and prey-specific behavioral and morphological changes in response to predator- and prey-specific risk.

The marked differences in predation risk posed by white sharks (Carcarodon carcarias) at island rookeries of Cape fur seals (Arctocephalus pusillus pusillus) offer a quasi‐experimental design within a natural system for exploring how prey adjust their behavior in response to temporal variation in predation risk. Here we compare movement of juvenile and adult Cape fur seals at a high risk (Seal Island) and low risk (Egg Island) rookery. We further compare juveniles and adults at Seal Island in low and high risk seasons and at low and high risk times of day within those seasons. Adult fur seals at Seal Island avoided traversing the zone of high white shark predation risk during the high risk period (0700–0959) in the season of high risk (winter), but not during the low risk season (summer). By contrast, adult fur seals at Egg Island showed no temporal discretion in either season. Unlike juvenile fur seals at Egg Island, juveniles at Seal Island adjusted their temporal movement patterns to more closely mimic adult seal movement patterns. This suggests that exposure to predators is the primary driver of temporal adjustments to movement by prey species commuting from a central place.

Predation is an important source of mortality in zooplankton but factors governing predation risk in marine food webs are still not well understood. Here, we examine the role of zooplankton behavior in determining predation risk. We first quantified motility of copepods with different feeding behaviors (ambush feeding, cruising, and feeding‐current feeding). Second, we estimated remote predator detection and escape characteristics of the studied copepods. Third, we proposed a simple behavior‐dependent encounter model to predict copepod predation risk from rheotactic predators. Finally, we compared our predictions with predation risk previously determined experimentally. For similar sized copepods, predicted predation risks were similar between feeding‐current feeders and cruising feeders, whereas predation was up to 8.5 times lower (range: 1.5–8.5) for ambush feeders. Predicted predation risks further differed between males and females depending on feeding behavior: in ambush feeders males actively search for non‐motile females and their predation risk was up to 6 times higher (range 1.2–6) than for females. In contrast, feeding current‐ and cruising feeders showed small differences in predation risk between genders. In all cases, predicted relative predation risks between particular behaviors were confirmed by empirical data from previous predation experiments. Our results demonstrate that prey behavior of zooplankton may lead to a predictable variation in predation risk from rheotactic predators of up to an order of magnitude, and therefore that individual behavior is an important factor in structuring zooplankton communities.

Prey behavioural traits within a population are commonly variable, unexpectedly so, given that predation is thought to be a strong selection pressure. This variation likely arises from complex, variable selection pressures, but experimental evaluations of prey responses to natural variability in selection pressures remain limited. We focus on the rock-pool-breeding mosquito Aedes vexans, which can influence the predation risk to its offspring through site selection for oviposition. We quantified the nature of selection pressures in the wild, i.e. the spatial and temporal variation in larval predation risk, by measuring densities of predatory dragonfly nymphs in rock pools along the mosquito breeding season. To examine the implication of selection pressure regimes for the evolution of oviposition site selection, we conducted manipulative experiments and measured female oviposition responses to variation in predation risk. Predation risk varied extensively over space and time; this variation showed both predictable and unpredictable elements. Females avoided large pools with permanent predators but appeared to show variable responses to medium-sized pools with unpredictable predation risk. We suggest that while it might be challenging to quantify complex selection environments and their impact on wild prey responses, more such studies can help explain puzzling variation in anti-predator responses.

Some organisms use morphological structures obtained by behavioural processes to lower mortality by predation. We test whether larvae of the limnephilid caddisfly Potamophylax latipennis (Curtis) vary their responses to the presence of different predators (dragonfly naiads, fire salamander larvae or brown trout) by choosing organic or mineral cases. We offered both case types to larvae, and simulated differences in predation risk using water conditioned with chemicals from the different predators. Our results show that Potamophylax larvae detect and discriminate predators using water-borne chemical cues and alter their choice of case type according to the perceived predation risk. Moreover, the distribution of larvae bearing cases of different anti-predator value matches the spatial variation in predation risk in the field.

Predation shapes communities through consumptive and non‐consumptive effects. In the latter case, prey respond to perceived predation risk through proactive or reactive risk management strategies occurring at different spatial and temporal scales. The predator–prey space race and landscape of fear concepts are useful to better understand how predation risk affects prey behavioral decisions and distribution. We assessed predation risk effects in a terrestrial Arctic community, where the arctic fox is the main predator of ground‐nesting birds. Using high‐frequency GPS data, we estimated a predator activity landscape corresponding to fox space use patterns and validated with an artificial prey experiment that this predator activity landscape correlated with the predation risk landscape. We then investigated the effects of the fox activity landscape on multiple prey species, by assessing the anti‐predator behavior of a main prey (snow goose) actively searched for by foxes, and the nest distribution of several incidental prey species. We first found that snow geese showed a stronger level of nest defense in areas highly used by foxes, possibly responding with a reactive strategy to variation in predation risk. Then, nests of incidental prey reproducing in habitats easily accessed by foxes had a lower probability of occurrence in areas highly used by foxes, suggesting these birds may use a proactive risk management strategy by shifting their distribution away from risky areas. For incidental prey species nesting in microhabitat refuges difficult to access by foxes, probability of nest occurrence was independent of predation risk in the surrounding area, as they avoid risk at a finer spatial scale. By tracking all individuals of the dominant predator species in our study area, we demonstrated the value of using predator space use patterns to infer spatial variation in predation risk. Overall, we highlight the diversity of risk management strategies in prey sharing a common predator, hence refining our understanding of the mechanisms driving species distribution and community structure.

The temporal niche has received less attention than the spatial niche in ecological research on free-ranging animals. Most studies that have examined the effect of season on the diel activity patterns of small mammals have been conducted in temperate climates where daily temperatures and day length are important predictors of activity. Extremely seasonal rainfall in northern Australia possibly exerts a strong influence on mammalian activity due to the influx of food resources. Using camera traps set over a 3-year period, we documented the diel activity patterns of 5 species of small mammals co-occurring on Groote Eylandt, in the wet-dry tropics of northern Australia. All species were strictly nocturnal but some responded differently to the effect of season. The northern quoll (Dasyurus hallucatus) displayed a bimodal activity pattern that did not differ between the seasons. The northern brown bandicoot (Isoodon macrourus) displayed bimodal activity in the wet season and unimodal activity in the dry. The more sustained activity of I. macrourus in the dry season may be the result of this species utilizing more cellulose-rich food in times of lower insect abundance, whereas D. hallucatus possibly exhibits lower dietary plasticity. The northern hopping-mouse (Notomys aquilo) was consistently active throughout the night in both seasons. Conversely, the delicate mouse (Pseudomys delicatulus) showed great plasticity in its nocturnal activity which altered significantly depending on both season and habitat. The disparity in activity pattern between these 2 rodents possibly reflects differences in predation risks. The grassland melomys (Melomys burtoni) was recorded only during the dry season in coastal grassland habitat, when its activity peaked sharply after nightfall. Our study highlights the interspecific variation in small mammal activity between the wet and dry seasons in northern Australia, which may be explained by differences in diet, habitat use, and predation risk in these species.

Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats

BackgroundPredation and predator abundance may significantly affect bird populations, especially ground nesting species, because nest predation is often the major cause of nest failure. Predator control by means of culling is frequently employed to benefit threatened prey species or to increase the abundance of small game species for hunting. The red fox (Vulpes vulpes), a generalist mesopredator of global relevance, is a major target of predator control. Commonly, in central Europe, red fox culling efforts intended to benefit prey species remain restricted to small areas. It is unclear, however, whether such restricted-area culling effectively lowers predation risk at a site or whether red fox abundance is more important than culling in shaping predation risk. We conducted an experiment using 273 camera supervised artificial nests at multiple study sites in clusters of hunting concessions with or without targeted fox culling in a fragmented montane forest landscape in Germany.ResultsUsing generalized additive models, we assessed whether incentivized recreational culling of red foxes was associated with local reductions in an index of predation risk and fox occurrence probability, or whether both were explained by red fox abundance instead. Final models indicated that restricted-area culling of red foxes was not associated with local reductions in predation risk, nor lower probability of a fox sighting, even for the plots with the largest hunting bags. Predation risk at a plot instead appeared to be driven by variation in the abundance of red foxes in the landscape surrounding the plots. After accounting for fox abundance, we found no additional relationship of artificial nest predation risk with landscape configuration.ConclusionsOur results imply that the scale and intensity of predator control achieved by incentivized recreational hunting was ineffective at altering fox abundance patterns and associated predation risk. We thus find no evidence to support incentives for uncoordinated recreational red fox culling as a conservation measure.

Predation risk is often associated with group formation in prey, but recent advances in methods for analysing the social structure of animal societies make it possible to quantify the effects of risk on the complex dynamics of spatial and temporal organisation. In this paper we use social network analysis to investigate the impact of variation in predation risk on the social structure of guppy shoals and the frequency and duration of shoal splitting (fission) and merging (fusion) events. Our analyses revealed that variation in the level of predation risk was associated with divergent social dynamics, with fish in high-risk populations displaying a greater number of associations with overall greater strength and connectedness than those from low-risk sites. Temporal patterns of organisation also differed according to predation risk, with fission events more likely to occur over two short time periods (5 minutes and 20 minutes) in low-predation fish and over longer time scales (>1.5 hours) in high-predation fish. Our findings suggest that predation risk influences the fine-scale social structure of prey populations and that the temporal aspects of organisation play a key role in defining social systems.

Prey living in risky environments can adopt a variety of behavioral tactics to reduce predation risk. In systems where predators regulate prey abundance, it is reasonable to assume that differential patterns of habitat use by prey species represent adaptive responses to spatial variation in predation. However, patterns of habitat use also reflect interspecific competition over habitat. Collared (Dicrostonyx groenlandicus) and brown (Lemmus trimucronatus) lemmings represent such a system and possess distinct upland tundra versus mesic meadow habitat preferences consistent with interspecific competition. Yet, we do not know whether this habitat preference might also reflect differences in predation risk or whether the two species differ in their behavioral tactics used to avoid predation. We performed experiments where we manipulated putative predation risk perceived by lemmings by increasing protective cover in upland and meadow habitats while we recorded lemming activity and behavior. Both lemming species preferentially used cover more than open patches, but Dicrostonyx was more vigilant than Lemmus. Both species also constrained their activity to protective patches in upland and meadow habitats, but during different periods of the day. Use of cover and vigilance were independent of habitat, suggesting that both species live in a fearsome but flattened landscape of fear at Walker Bay (Nunavut, Canada), and that their habitat preference is a consequence of competition rather than predation risk. Future studies aiming to map the contours of fear in multi-prey–predator systems should consider how predation and competition interact to modify prey species’ habitat preference, patch use, and vigilance.

We examined the importance of sex differences in predation risk in generating sexual segregation in the guppy, Poecilia reticulata. We hypothesised that sex differences in predation risk will result in habitat segregation and ultimately social segregation of the sexes, with the more vulnerable sex (males in this case) using safer habitats. In accordance with the predation risk hypothesis we observed sexual segregation in a population associated with high but not low predation risk. Under high predation risk we observed a larger proportion of males in shallow marginal habitats resulting in habitat segregation and ultimately social segregation of the sexes. Furthermore, habitat segregation by sex was associated with habitat segregation by body length with shoals in deeper water having a larger mean body length. Shoaling fish species have been key models in investigating group living, and further research directed towards understanding sexual segregation in other fish species would be valuable.

Intimidating courtship and sex differences in predation risk lead to sex-specific behavioural syndromes

Food availability and temporal variation in predation risk are both important determinants of the magnitude of antipredator responses, but their effects have rarely been examined simultaneously, particularly in wild prey. Here, we determine how food availability and long-term predation risk affect antipredator responses to acute predation risk by monitoring the foraging response of free-ranging snowshoe hares (Lepus americanus) to an encounter with a Canada lynx (Lynx canadensis) in Yukon, Canada, over four winters (2015-2016 to 2018-2019). We examined how this response was influenced by natural variation in long-term predation risk (2-month mortality rate of hares) while providing some individuals with supplemental food. On average, snowshoe hares reduced foraging time up to 10h after coming into close proximity (≤75m) with lynx, and reduced foraging time an average of 15.28±7.08min per lynx encounter. Hares tended to respond more strongly when the distance to lynx was shorter. More importantly, the magnitude of hares' antipredator response to a lynx encounter was affected by the interaction between food-supplementation and long-term predation risk. Food-supplemented hares reduced foraging time more than control hares after a lynx encounter under low long-term risk, but decreased the magnitude of the response as long-term risk increased. In contrast, control hares increased the magnitude of their response as long-term risk increased. Our findings show that food availability and long-term predation risk interactively drive the magnitude of reactive antipredator response to acute predation risk. Determining the factors driving the magnitude of antipredator responses would contribute to a better understanding of the indirect effects of predators on prey populations.

Temporal variation in predation risk may be an important determinant of prey antipredator behaviours. According to the risk allocation hypothesis, the strongest antipredator behaviours are expected when periods of high risk are short and infrequent. We tested this prediction in a laboratory experiment where common frog Rana temporaria tadpoles were raised form early larval stages until metamorphosis. We manipulated the time a predatory Aeshna dragonfly larva was present and recorded behavioural responses (activity) of the tadpoles at three different time points during the tadpoles’ development. We also investigated how tadpole shape, size and age at metamorphosis were affected by temporal variation in predation risk. We found that during the two first time points activity was always lowest in the constant high‐risk situation. However, antipredator response in the two treatments with brief high‐risk situation increased as tadpoles developed, and by the third time point, when the tadpoles were close to metamorphosis, activity was as low as in the constant high‐risk situation. Exposure to chemical cues of a predation event tended to reduce activity during the first time period, but caused no response later on. Induced morphological changes (deeper tail and shorter relative body length) were graded the response being stronger as the time spent in the proximity of predator increased. Tadpoles in the brief risk and chemical cue treatments showed intermediate responses. Modification of life history was only found in the constant high‐risk treatment in which tadpoles had longer larval period and larger metamorphic size. Our results indicate that both behavioural and morphological defences were sensitive to temporal variation in predation risk, but behaviour did not respond in the manner predicted by the risk allocation model. We discuss the roles of concentration of predator chemical cues and prey stage‐dependency in determining these responses.