Perceived Predation Risk Research Articles

Background choice and immobility as context dependent tadpole responses to perceived predation risk

The association of immobility and camouflage is widespread as a defensive mechanism in prey from varied taxa. However, many experiments assessing the reaction of prey to predator cues are conducted under artificial laboratory conditions. In a previous experiment we observed the tadpoles of Ololygon machadoi (Hylidae) to respond to predator visual and/or chemical cues by choosing backgrounds that improve their disruptive properties, but detected no associated reduction of movement. Here we experimentally demonstrate this response in the species' natural habitat, on backgrounds where the tadpoles are likely to achieve their best camouflage. We also tested whether previous experiences could influence both background choice and immobility in O. machadoi tadpoles. These novel experimental results suggest that a defensive behavior—i.e., reduction of movement—in these tadpoles is more strongly expressed under the natural conditions where they evolved, compared to laboratory conditions where prey and predator were brought into closer contact. Besides, previous experiences are likely to play an important role in expressed defensive responses.

“The tale of the three little tits”: Different nest building solutions under the same environmental pressures

Evolutionary selection pressures, and species-specific ecology and behavior, promote a great variability in the size and composition of nests. However, it would be expected that phylogenetically close species, with similar ecological needs, breeding at the same time in the same place, would also build similar nests. In contrast with this, previous studies have found differences in nest mass and composition among closely related sympatric species. These differences have been attributed to small differences in body size (smaller species building larger and/or more insulated nests), or to the different ways in which species perceive the environment (e.g. perceived predation risk). In this study, for the first time, we searched for differences between nest mass, composition, and importance of the different functional parts of the nest between Blue ( Cyanistes caeruleus), Great ( Parus major) and Coal tits ( Periparus ater) breeding under the same conditions. We found that smaller species built larger nests and/or include more thermoregulatory materials, probably having greater insulating capacity, which agrees with previous hypotheses. In particular, Blue Tits made greater use of bark, feathers and vegetable fiber, while Great Tits used wild boar hair in greater proportions. In addition, for the first time, we described in detail the nest composition of Coal Tits, which contained large amounts of fluff compared to the other two species. All these results are in line with previous hypothesis linking nest size and composition to the size of the birds, and the existence of species-specific characteristics in the selection of materials for nest building.

Maternal predation risk increases offspring’s exploration but does not affect schooling behavior

Abstract The environment that parents experience can influence their reproductive output and their offspring’s fitness via parental effects. Perceived predation risk can affect both parent and offspring phenotype, but it remains unclear to what extent offspring behavioral traits are affected when the mother is exposed to predation risk. This is particularly unclear in live-bearing species where maternal effects could occur during embryogenesis. Here, using a half-sib design to control for paternal effects, we experimentally exposed females of a live-bearing fish, the guppy (Poecilia reticulata), to visual predator cues and conspecific alarm cues during their gestation. Females exposed to predation risk cues increased their antipredator behaviors throughout the entire treatment. Offspring of mothers exposed to the predation stimuli exhibited more pronounced exploratory behavior, but did not show any significant differences in their schooling behavior, compared to controls. Thus, while maternally perceived risk affected offspring’s exploration during early stages of life, offspring’s schooling behavior could be influenced more by direct environmental experience rather than via maternal cues. Our results suggest a rather limited role in predator-induced maternal effects on the behavior of juvenile guppies.

Mammalian nest predation induces small-scale nest site switching in territorial tawny owl (Strix aluco) females

Nest predation is a major factor affecting fitness in birds. Individuals are expected to respond to nest predation by selecting safe nesting sites and by moving away from risky sites. Thereby, perceived risk or experience of predation should lead to shifts in nest site selection. Experimental studies on behavioural and life-history consequences of nest predation have traditionally manipulated the risk of predation and studied the immediate consequences thereof. Fewer studies have however analysed the behavioural consequences of perceived predation risk to future breeding events and we know little about how sedentary territorial species respond to nest predation. We experimentally manipulated tawny owl (Strix aluco) breeding nest site choice by providing an additional alternative nest box within the territory, nearby the original nesting sites. The new nest box was provided either after a successful reproductive event (control group), or following a failed reproductive event caused by a nest predator (i.e. pine marten Martes martes, predated group).

A question of size and fear: competition and predation risk perception among frugivores and predators

Abstract Mammalian spatial and temporal activity patterns can vary depending on foraging behavior or the perception of predation or competition risk among species. These behaviors may in turn be altered by human influences such as defaunation. Herein, we evaluate whether frugivores avoid areas with high visitation rates by potential predators or competitors, and whether this avoidance changes in areas with different degrees of defaunation. We installed 189 cameras under fruit trees in six areas of the Atlantic Forest, Brazil, that differ in the abundance of top predators and large frugivores. Small predators and small frugivores were more frequent at night while large frugivores were more frequent during the day, but small frugivores visited and spent less time at fruiting trees on brighter nights, unlike large predators and large frugivores. Small frugivores also were less frequent in areas with high visitation by large frugivores and more frequent in highly defaunated areas. Our results suggest that the dynamics among mammalian functional groups varied according to diel patterns, potential competitors, and defaunation. We highlight the importance of understanding how species interactions are changing in areas exposed to strong human impacts to mitigate the indirect effects of defaunation.

Mixed-species herding levels the landscape of fear

Prey anti-predator behaviours are influenced by perceived predation risk in a landscape and social information gleaned from herd mates regarding predation risk. It is well documented that high-quality social information about risk can come from heterospecific herd mates. Here, we integrate social information with the landscape of fear to quantify how these landscapes are modified by mixed-species herding. To do this, we investigated zebra vigilance in single- and mixed-species herds across different levels of predation risk (lion versus no lion), and assessed how they manage herd size and the competition-information trade-off associated with grouping behaviour. Overall, zebra performed higher vigilance in high-risk areas. However, mixed-species herding reduced vigilance levels. We estimate that zebra in single-species herds would have to feed for approximately 35 min more per day in low-risk areas and approximately 51 min more in high-risk areas to compensate for the cost of higher vigilance. Furthermore, zebra benefitted from the competition-information trade-off by increasing the number of heterospecifics while keeping the number of zebra in a herd constant. Ultimately, we show that mixed-species herding reduces the effects of predation risk, whereby zebra in mixed-species herds, under high predation risk, perform similar levels of vigilance compared with zebra in low-risk scenarios.

Better safe than sorry: The response to a simulated predator and unfamiliar scent by the European hare

AbstractPredator presence can create a “landscape of fear,” which is defined as the spatially explicit distribution of perceived predation risk as seen by prey. Prey species can alter their behavior and space use as a response to increased predation risk, which might be traded off with energetic requirements. Thus, whether or not an anti‐predator behavior is performed might depend on the perceived risk. In this study, we investigated the behavioral and spatial response of the European hare (Lepus europaeus) toward the presence of a predator scent, using red fox (Vulpes vulpes) scat, an unfamiliar control scent (butyric acid), and a true control (no scent). We collected data on hare activity times and behavior using 50 camera trap locations and spatial data using GPS telemetry (30,481 GPS positions of 12 hares). Hares showed spatial anti‐predator behaviors within their home range, for example, the local avoidance of areas treated with scent and remaining further from field edges, in response to sympatric predator scent and partly also in response to unfamiliar butyric acid. Conversely, more costly anti‐predator behaviors, that is, increased vigilance at the expense of foraging, were only shown in response to the predator scent. Our results suggest that prey species respond flexibly toward scent cues, utilizing less costly anti‐predator behaviors independent of the perceived threat, whereas costly anti‐predator responses are only used in the presence of “real” threat. Further, our findings emphasize that a combination of camera trap and GPS data can provide detailed information on animal behavior and space use, and caution that interpretation of one data source alone might lead to incomplete conclusions.

Disturbance cues as a source of risk assessment information under natural conditions

Abstract Disturbance cues are released by stressed or disturbed prey prior to a predator attack and convey useful risk assessment information regarding local threats. While studies have shown that disturbance cues may be important early on within the predation sequence (prior to an attack), their role in predator–prey interactions remains relatively overlooked by ecologists. Critically, experimental studies examining disturbance cues, especially among prey fishes, have been conducted primarily under laboratory or semi‐natural conditions. Here, we tested the prediction that disturbance cues function as sources of risk assessment information in situ. We exposed Trinidadian guppies, in two natural populations differing in predation risk, to a model predator paired with stream water or the disturbance cue collected from guppies from either a high‐ or low‐predation risk population. We found that the predator inspection response of guppies to disturbance cues depends on the level of risk of both the focal and the cue source population. Guppies from both populations exhibited increased latencies to inspect, lower inspection rates and reduced inspecting group sizes towards the model paired with conspecific disturbance cues versus a stream water control. Interestingly, guppies of both populations showed evidence of higher perceived predation risk towards the disturbance cues collected from high‐predation risk donors compared to low‐predation risk donors. Our results support the hypothesis that disturbance cues function as a source of information used by prey fish in the assessment of predation risk and provide the first evidence of disturbance cue function under fully natural conditions.

Moonlight rather than moon phase influences activity and habitat use in an invasive amphibian predator and its native amphibian prey

Predation affects population dynamics via both direct mortality and behavioural responses to the threat of death. Environmental factors are known to influence the activity of both predator and prey in amphibians by interacting with their physiological constraints. For instance, lunar cues (moonlight and moon cycle) influence amphibian predation risk and foraging efficiency. However, little information is available on how the moonlight affects activity and habitat use. Here, we investigated whether lunar light flux, environmental variables, and lunar phases influence abundance and habitat use in a predator-prey system consisting of an invasive predator (i.e., the American bullfrog Lithobates catesbeianus) and a native prey (i.e., the green frogs Pelophylax spp.). In accordance with both the “visual acuity” and “predation risk” hypotheses, the activity of the invasive predator was enhanced in moonlit nights, especially in open habitats, whereas the activity of the native prey species seemed to be not affected by the intensity of moonlight. Contrary to the “habitat-mediated predation risk hypothesis”, no suppressive effect of moonlight in open habitats was found for L. catesbeianus, this possibly evidencing the lack of perceived predation risk by this alien species. Moon cycle had no effect on American bullfrog abundance and weakly affected the activity of green frogs especially in open habitats between the first quarter and the full moon. Our study shows how moonlight, lunar phases and environmental parameters influence the behaviour and ecology of the American bullfrog and one of its native prey. Since indirect effects have the potential to moderate or amplify the impacts of invasive species on native populations, our findings could help to understand the spreading of American bullfrogs and to possibly mitigate their impacts on native fauna through habitat restoration.

Maternal predator-exposure affects offspring size at birth but not telomere length in a live-bearing fish.

The perception of predation risk could affect prey phenotype both within and between generations (via parental effects). The response to predation risk could involve modifications in physiology, morphology, and behavior and can ultimately affect long‐term fitness. Among the possible modifications mediated by the exposure to predation risk, telomere length could be a proxy for investigating the response to predation risk both within and between generations, as telomeres can be significantly affected by environmental stress. Maternal exposure to the perception of predation risk can affect a variety of offspring traits but the effect on offspring telomere length has never been experimentally tested. Using a live‐bearing fish, the guppy (Poecilia reticulata), we tested if the perceived risk of predation could affect the telomere length of adult females directly and that of their offspring with a balanced experimental setup that allowed us to control for both maternal and paternal contribution. We exposed female guppies to the perception of predation risk during gestation using a combination of both visual and chemical cues and we then measured female telomere length after the exposure period. Maternal effects mediated by the exposure to predation risk were measured on offspring telomere length and body size at birth. Contrary to our predictions, we did not find a significant effect of predation‐exposure neither on female nor on offspring telomere length, but females exposed to predation risk produced smaller offspring at birth. We discuss the possible explanations for our findings and advocate for further research on telomere dynamics in ectotherms.

Comparative Analysis of Anti-predator Behaviour and Life History Traits of the Tadpoles Exposed to Predation Risk and Corticosterone

Anuran tadpoles show behavioural and morphological alterations in the presence of predatory cues (perceived predation risk). Recent studies suggested the possible role of stress hormone corticosterone (CORT) in anti-predator responses. We speculated that the anti-predator responses of prey tadpoles exposed to predation risk and CORT will be similar if they are mediated through CORT. In the present study, we compared behavioural and life history responses of Duttaphrynus melanostictus tadpoles exposed to (i) predatory tadpoles of Hoplobatrachus crassus, and (ii) two concentrations (1 and 10 µg/L) of CORT. The results revealed that exposure of the tadpoles to predation risk and CORT have similar effects on behaviour and life history traits. Tadpoles exposed to predation risk and CORT did not alter behaviour in response to alarm cues. Tadpoles exposed to predation risk and different concentrations of CORT delayed metamorphosis with a reduction in size. CORT influenced metamorphosis and size of the tadpoles in concentration dependent manner. These results suggest that the presence of non-lethal predators affects life history traits possibly through the stress hormone.

Habitat influence on activity patterns of brush-tailed rock-wallabies in Queensland

The brush-tailed rock-wallaby (Petrogale penicillata) is a nocturnal refuge dependent herbivore that can be found from south-east Queensland to East Gippsland in Victoria. Brush-tailed rock-wallaby colonies are situated in many different habitat types, and refuge within this habitat is important for their survival. Dingoes coexist with P. penicillata and are perceived to be a threat. This study aimed to determine the link between habitat and P. penicillata behaviour and their interaction with predators. Three P. penicillata colonies were studied within the Little Liverpool Range, Queensland. Images of P. penicillata and dingoes from camera traps were analysed for daily activity patterns and activity overlap between species. Dingo scats were collected and analysed to determine predation. The results indicated that different habitat types change the perceived predation risk and corresponding activity patterns of P. penicillata. Predation risk impacted foraging behaviour, with rock-wallabies in exposed habitat types exhibiting greater predator avoidance behaviours than those in more protected habitat types. The results indicate that brush-tailed rock-wallabies modified their activity patterns according to different habitat types to reduce their risk of predation.

Experimental manipulation of perceived predation risk and cortisol generates contrasting trait trajectories in plastic crucian carp.

Most animals constitute potential prey and must respond appropriately to predator-mediated stress in order to survive. Numerous prey also adaptively tailor their response to the prevailing level of risk and stress imposed by their natural enemies, i.e. they adopt an inducible defence strategy. Predator exposure may activate the stress axis, and drive the expression of anti-predator traits that facilitate survival in a high-risk environment (the predation-stress hypothesis). Here, we quantified two key morphological anti-predator traits, body morphology and coloration, in crucian carp reared in the presence or absence of a predator (pike) in addition to experimental manipulation of physiological stress via implants containing either cortisol or a cortisol inhibitor. We found that predator-exposed fish expressed a deeper-bodied phenotype and darker body coloration as compared with non-exposed individuals. Skin analyses revealed that an increase in the amount of melanophores caused the dramatic colour change in predator-exposed fish. Increased melanization is costly, and the darker body coloration may act as an inducible defence against predation, via a conspicuous signal of the morphological defence or by crypsis towards dark environments and a nocturnal lifestyle. By contrast, the phenotype of individuals carrying cortisol implants did not mirror the phenotype of predator-exposed fish but instead exhibited opposite trajectories of trait change: a shallow-bodied morphology with a lighter body coloration as compared with sham-treated fish. The cortisol inhibitor did not influence the phenotype of fish i.e. neither body depth nor body coloration differed between this group and predator-exposed fish with a sham implant. However, our results illuminate a potential link between stress physiology and morphological defence expression.

Differences in perceived predation risk associated with variation in relative size of extra-pair and within-pair offspring.

Extra-pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra-pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra-pair and within-pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer-winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer-winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra-pair and within-pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.

High perceived predation risk during development affects mutual mate choice in a cichlid fish

Predicting patterns of variation in sexual traits requires understanding how developmental environments influence mate choice. Here, we studied how long-term perceived high predation risk affects mutual mate choice in the cichlid Pelvicachromis taeniatus. From hatching onwards, fish were exposed regularly to either conspecific alarm cues signalling high risk or a control treatment consisting of exposure to water. Alarm cue-exposed and control adult fish were then offered the dichotomous choice between opposite-sex fish from different treatment groups. Under chronic predation risk, lower investment in mate choice and assortative preferences for mates from the same environment may be optimal. As predicted, alarm cue-exposed males assessed potential mates less than controls whereas females did not. Mate preferences differed as well but were independent of sex. While alarm cue-exposed fish were unselective, against expectations, control fish displayed disassortative preferences for alarm cue-exposed fish. This indicates that perceived high predation risk during development may contribute to maintaining variation in mating preferences and sexual traits.

Preferences for and use of light microhabitats differ among and within populations of a polytypic poison frog

Abstract Anti-predator strategies can influence trade-offs governing other activities important to fitness. Crypsis, for example, might make conspicuous sexual display especially costly, whereas aposematism might reduce or remove such costs. We tested for correlates of anti-predator strategy in Oophaga pumilio, a polytypic poison frog with morphs spanning the crypsis–aposematism continuum. In the wild, males of visually conspicuous morphs display from conspicuous perches and behave as if they perceive predation risk to be low. We thus predicted that, given a choice of ambient light microhabitats, these males would use high ambient light conditions the most and be most likely to perch in high-light conditions. We found no evidence that differently colored male O. pumilio preferentially used bright microhabitats or that ambient light influenced perching in a morph-specific manner. Independent of light conditions, males from the most conspicuous population perched the least, but the most conspicuous individuals from a polymorphic population perched the most. These patterns suggest that preferences do not necessarily underlie among-morph differences observed in the wild. This could be explained, and remain consistent with theory, if risk aversion is shaped, in part, by experience.

Shrub cover homogenizes small mammals\u2019 activity and perceived predation risk

Altered disturbance regimes, increasing atmospheric CO2, and other processes have increased woody cover and homogenized vegetation in savannas across the planet. African savannas with extensive versus minimal woody cover often have vastly different animal communities. However, we lack a clear mechanistic understanding of why animal communities are changing with vegetation structure. Our goal for this study was to understand how vegetation structure in an African savanna shaped the perceived predation risk of small mammals, hence affecting their activity. Using a reciprocal measure of standard giving-up-densities, amount of food eaten, we found sharp declines in rodents’ perceived predation risk and increased rodent activity underneath shrub cover. This response was consistent across species; however, species showed subtle differences in their responses to grassy vegetation. Our findings suggest that areas of minimal or extensive shrub cover (shrub encroachment) may be homogenizing rodents’ perceptions of predation risk and thus shaping their use of space.

Intermediate turbidity elicits the greatest antipredator response and generates repeatable behaviour in mosquitofish

Increased turbidity, a common human-induced aquatic disturbance, can potentially have major impacts on predator–prey interactions via effects on key foraging and antipredator behaviours, on the repeatability of these behaviours (i.e. on animal personalities) and on behavioural syndromes (correlations among behaviours). Here, we repeatedly assayed individual western mosquitofish, Gambusia affinis, across a range of turbidity levels (low, intermediate, high) to test the degree to which a suite of behaviours (activity, exploration, sociality, responses to olfactory predator cues) scaled with increasing turbidity. In particular, we tested the a priori hypothesis, based on previous work, that fish show stronger behavioural repeatability and behavioural correlations when perceived predation risk is high. While individuals in all treatments responded to predator cues by reducing activity and exploration, those assayed in intermediate turbidity exhibited the strongest antipredator responses. Consistent with our prediction that repeatability should be greatest in high risk, significant behavioural repeatability was only detected in antipredator behaviours at intermediate turbidity. Significant correlations among behavioural traits were detected in all turbidity treatments but primarily under threat of predation – not when predator cues were absent (with one exception). This study demonstrates that levels of human-induced environmental change may interact with predation risk to shape both mean behavioural responses as well as patterns of behavioural correlations within and among individuals.

The risk of ignoring fear: underestimating the effects of habitat loss and fragmentation on biodiversity

CONTEXT: Habitat loss and fragmentation threaten species not only through structural landscape changes and resource reduction, but also through modifications to species’ interactions. In particular, the observed consequences of landscape changes for predator–prey interactions often lack a clear pattern, indicating a range of complex behavioral adaptations and interactions. One potentially important contributing factor shaping these consequences is perceived predation risk and hence fear, which is rarely explicitly addressed in studies on habitat modification. OBJECTIVES: We investigated how fear changes prey community structures under habitat loss and fragmentation and identified habitat properties driving these changes. METHODS: We applied a spatially-explicit, individual-based model which simulates home range formation of a mammalian prey community based on food availability and perceived predation risk. With the model we predicted prey community structures under different landscape scenarios. RESULTS: Fear intensified the negative effects of habitat loss and fragmentation on prey communities, causing a non-proportional diversity loss of up to 30%. Shifts in community composition from large to small animals were reinforced. The highest prey diversity was supported in landscapes with non-fragmented safe areas. Our findings highlight the importance of fear in shaping prey community structures under conditions of landscape change. CONCLUSIONS: Our modelling approach addresses the mechanisms that link individual space use with community structure. It reveals the key role played by the spatial distribution of safe patches in mitigating the negative effects of landscape changes. Thereby, it supports modern conservation efforts that go beyond single-species approaches by taking changes in community structure into account.

Variation in anti-predator behaviors of white-tailed deer (Odocoileus virginianus) in a multi-predator system

Anti-predator responses to perceived predation risk can influence population demography. Understanding the relative effect of predator exposure and intraspecific interactions across a variety of anti-predator behaviors provides important insight into inter- and intra-specific drivers of species-specific behaviors. We merged classical behavioral observation methods with camera trapping techniques to examine anti-predator behaviors of white-tailed deer (Odocoileus virginianus (Zimmermann, 1780)) relative to variation in predator exposure and interspecific interactions. We coded 772 behavioral observations from >180 000 images spanning 605 trap-nights. Seasonal differences in behavioral responses to diminishing returns on foraging effort indicated that deer are risk-averse foragers and are more likely to exhibit risky behaviors in the presence of a concentrated food resource when the nutritional value of food resources are high. However, deer tended to spend less time at a site as resources diminished, supporting marginal value theories of habitat use. Intraspecific interaction predicted vigilance and the amount of time spent at a site. Similar to many other species, deer tended to be less vigilant and spend more time at a site as group size increased. Our research suggests that white-tailed deer in Wisconsin make foraging decisions based on factors associated with individual fitness, presence of conspecifics, and habitat characteristics.