The predation risks of interspecific eavesdropping: weasel–vole interactions

Competing species benefit from eavesdropping on each other's signals by learning about shared resources or predators. But conspicuous signals are also open to exploitation by eavesdropping predators and should also pose a threat to other sympatric prey species. In western Finland, sibling voles Microtus rossiameridionalis and field voles M. agrestis compete for food and space, and both species rely upon scent marks for intraspecific communication. Both vole species are prey to a range of terrestrial scent hunting predators such as least weasels, however, the competitively superior sibling voles are taken preferentially. We tested in large out‐door enclosures whether field voles eavesdrop on the signals of its competitor, and whether they behave as though this eavesdropping carries a risk of predation. We presented field voles with scent marks from unknown conspecifics and sibling voles and measured their visitation, activity and scent marking behaviours at these scents under high (weasel present) and low (weasel absent) predation risk. Field voles readily visited both field and sibling vole scents under both high and low predation risk; however their activity at sibling vole scent marks declined significantly under increased predation risk. In contrast, predation risk did not affect field voles’ activity at conspecific scents. Thus, field voles were compelled to maintain eavesdropping on heterospecific scents under an increased risk of predation, however they compensated for this additional risk by reducing their activity at these risky scents. Scent marking rates declined significantly under high predation risk. Our results therefore reveal a hidden complexity in the use of social signals within multi‐species assemblages that is clearly sensitive to the potential for increased predation risk. The predation risks of interspecific eavesdropping demonstrated here represents a significant generalisation of the concept of associational susceptibility.     

Predators Are Attracted to the Olfactory Signals of Prey

Background

Predator attraction to prey social signals can force prey to trade-off the social imperatives to communicate against the profound effect of predation on their future fitness. These tradeoffs underlie theories on the design and evolution of conspecific signalling systems and have received much attention in visual and acoustic signalling modes. Yet while most territorial mammals communicate using olfactory signals and olfactory hunting is widespread in predators, evidence for the attraction of predators to prey olfactory signals under field conditions is lacking.

Methodology/Principal Findings

To redress this fundamental issue, we examined the attraction of free-roaming predators to discrete patches of scents collected from groups of two and six adult, male house mice, Mus domesticus, which primarily communicate through olfaction. Olfactorily-hunting predators were rapidly attracted to mouse scent signals, visiting mouse scented locations sooner, and in greater number, than control locations. There were no effects of signal concentration on predator attraction to their prey''s signals.

Conclusions/Significance

This implies that communication will be costly if conspecific receivers and eavesdropping predators are simultaneously attracted to a signal. Significantly, our results also suggest that receivers may be at greater risk of predation when communicating than signallers, as receivers must visit risky patches of scent to perform their half of the communication equation, while signallers need not.     

Dangerous liaisons: the predation risks of receiving social signals

Individuals are at risk when communicating because conspicuous signals attract both conspecifics and eavesdropping predators. This predation cost of communicating has typically been attributed to signalling individuals because of their conspicuous role, and is a core concept within sexual selection and communication ecology. But, if predators are attracted to signals, then receivers, both intended or otherwise, may also find themselves at risk of predation. Here, we review the theoretical basis and empirical evidence that receiving also carries a risk of predation. We distinguish between the risks of receiving and responding to signals, and we argue that receivers of signals that are long lived, are highly predictable in time or place and/or cannot be received quickly are likely to be at greater risk of predation compared to receivers of signals without these properties. We review recent empirical evidence from a variety of taxa that supports the hypothesis that receivers (including heterospecific prey) are aware of these risks and that they modify their behaviour to balance the risks against the benefits of receiving under predation threat. We also discuss the wider implications of risky receiving for receiving and signalling behaviour in prey, as well as for the prey's predators.     

Potential risks of olfactory signaling: the effect of predators on scent marking by beavers

Mammals scent mark their territories to advertise occupancyand ownership. However, signaling with scent for territorialdefense can have a negative effect by advertising an individual'spresence and location to predators. In this study, we measuredresponses to a simulated territorial intrusion by conspecificadult male Eurasian beavers (Castor fiber) either in the localizedpresence or in the absence of odor of a predator to test thehypothesis that the territorial defense of free-living beaverswould be disrupted by the presence of predation risk in theirnatural environment. We predicted that beavers would significantlyreduce their willingness to countermark intruder's scent inthe presence of the scent of predators (wolf [Canis lupus] andlynx [Lynx lynx]), compared with a control (no odor), as responsesare in general stronger to predator scent marks than nonpredatorscent. Therefore, we also predicted that the effects of nonpredatorymammal scent (neophobic control) (eland [Taurotragus oryx] andhorse [Equus cabalus]) are to be expected somewhere in betweenthe effects of the predator odor and a control. Our resultssuggest that both predator and nonpredator scents reduce beaversresponse to a simulated intruder's scent mounds and thereforedisrupt their territorial defense. However, predator scent hada stronger effect than nonpredator scent. Beavers may thereforebe at great risk on territories with predators present becauseof the trade-off between predator avoidance and territorialdefense. Our study demonstrates the potential of predation riskas a powerful agent of counterselection on olfactory signalingbehavior.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Anti-predator behaviour changes following an aggressive encounter in the lizard Tropidurus hispidus

Avoiding predators may conflict with territorial defence because a hiding territorial resident is unable to monitor its territory or defend it from conspecific intrusions. With persistent intruders, the presence of an intruder in the near past can indicate an increased probability of future intrusions. Therefore, following a conspecific-intrusion, territorial residents should minimize costs from future intrusions at the cost of higher predation risks. I conducted experiments with males of the territorial lizard Tropidurus hispidus recording approach distance (distance between predator and prey when the prey escapes) and time to re-emergence from a refuge after hiding. Past aggressive interactions affected anti-predator behaviour: lizards re-emerged sooner (compared to a control) when the predator attacked 5 min after an aggressive encounter. If the predator attacked while an aggressive encounter was ongoing, there was also a reduction in approach distance. The results are consistent with an economic hypothesis which predicts that T. hispidus incur greater predation risks to minimize future territorial intrusion; additionally they show that the effects of past and ongoing aggressive interactions are different, consistent with the minimization of present intrusion costs. These results are relevant for studies of the changes in aggressive behaviour due to changes in the social environment and for studies of the costs and (co) evolution of aggressive and anti-predator strategies.     

Feeling Vulnerable? Indirect Risk Cues Differently Influence How Two Marsupials Respond to Novel Dingo Urine

In Tasmania, introduced predators are becoming more common. How Tasmanian prey respond to novel predator cues is of particular interest for their survival and management. Prey response to predator scents may depend on whether predator and prey share an evolutionary history and may be influenced by indirect risk cues such as perceived shelter or safety in the environment. To simultaneously explore the effects of indirect and direct risk cues (predator scent) on free‐living Tasmanian pademelons (Thylogale billardierii) and brush tail possums (Trichosurus vulpecula), we placed dingo (Canis lupus dingo) urine scents inside and outside a 25 ‐m² selective feeding enclosure to mimic a heterogeneous risk landscape. Despite the lack of a historical relationship between dingoes and Tasmanian fauna, pademelons and possums demonstrated flight and vigilance when confronted with the novel scent outside the enclosure. According to our index of deterrence, number of successful entries/approaches, both species were deterred. However, responses inside the safe enclosure differed according to species. For instance, pademelons made more approaches/entries into the enclosure and fled more following approaches to scent marks both inside and outside the enclosure. In comparison, possums only exhibited similar responses outside the enclosure, and there was no effect of stimulus inside the safe compound. Our findings suggest that small animals may be pre‐adapted to avoid some predators they have not previously been in contact with, and that brush tail possums are more likely to respond to predation cues when exposed and vulnerable. Ultimately, the cumulative effects of direct and indirect risk cues may either increase or reduce a repellent response.     

Do scent marks increase predation risk of microtine rodents?

Reproductive activities, including signalling with scents, may increase the risk of predation. Mammalian predators, like small mustelids, find voles by using odour cues of scent marks. Scent marks are also visible in ultraviolet light, and at least some diurnal raptors are attracted to these markings in the field. We performed a field experiment to find out whether manipulation of scent markings affects the density, survival and mobility of free-living voles, and the activity of mammalian and avian predators. A total of 20 plots (each 1 ha) were randomly divided into two treatments: scent manipulation and control plots. Scent manipulation plots were treated with vole scent-liquid and control plots with water. From each plot 1–2 voles were radio-collared and tracked for three weeks. Predators hunted more often on scent manipulation plots than on control plots leading to lower survival time of voles. Although scent manipulation attracted more avian predators, small mustelids were the main predators of voles. The density or the mobility of voles did not differ significantly between manipulation and control plots. Our results suggest that odour of scent marks may be a larger risk to voles than UV visibility of scent marks.     

Nonlinearity in the predation risk of prey mobility

Odorous waste products such as urine and faeces are unavoidable for most animals and are widely exploited by predators and their prey. Consequently, waste accumulations can be risky and prey which increase their mobility in order to disperse and dilute their waste should avoid a high predation risk until this benefit is balanced by the increasing risks of random predator encounter. This hypothesis was tested for voles (Microtus spp.) in Finland which are vulnerable to predation due to the scent and ultraviolet attractiveness of their urine. The mortality and mobility of radio-collared voles showed a U-shaped relationship, regardless of vole sex, species or population cycle phase. The low risks for prey making intermediate movements suggest that predation risk can exert strong selective pressures on prey such that they have little respite from the risk of being killed.     

Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.     

Spatial Partitioning of Predation Risk in a Multiple Predator-Multiple Prey System

ABSTRACT Minimizing risk of predation from multiple predators can be difficult, particularly when the risk effects of one predator species may influence vulnerability to a second predator species. We decomposed spatial risk of predation in a 2-predator, 2-prey system into relative risk of encounter and, given an encounter, conditional relative risk of being killed. Then, we generated spatially explicit functions of total risk of predation for each prey species (elk [Cervus elaphus] and mule deer [Odocoileus hemionus]) by combining risks of encounter and kill. For both mule deer and elk, topographic and vegetation type effects, along with resource selection by their primary predator (cougars [Puma concolor] and wolves [Canis lupus], respectively), strongly influenced risk of encounter. Following an encounter, topographic and vegetation type effects altered the risk of predation for both ungulates. For mule deer, risk of direct predation was largely a function of cougar resource selection. However, for elk, risk of direct predation was not only a function of wolf occurrence, but also of habitat attributes that increased elk vulnerability to predation following an encounter. Our analysis of stage-based (i.e., encounter and kill) predation indicates that the risk effect of elk shifting to structurally complex habitat may ameliorate risk of direct predation by wolves but exacerbate risk of direct predation by cougars. Information on spatiotemporal patterns of predation will be become increasingly important as state agencies in the western United States face pressure to integrate predator and prey management.     

Scent-marking by male mice under the risk of predation

The use by predators of scent marks made by potential prey isa largely unexplored potential cost of olfactory signaling.Here we investigate how animals that differ in their investmentin scent-marking respond to simulated predation risk, by comparingthe willingness to approach and counter-mark the scent marksof a competitor in the presence or absence of predator odor.We aimed to test whether animals that invest heavily in scent-marking,and which may thus be more vulnerable to eavesdropping predators,will either (1) take greater risks to counter-mark the competitor'sscent or (2) reduce or abandon scent-marking. Using outbredmale laboratory mice, Mus musculus, we show that, in the absenceof predators, individuals which initially scent-mark at highfrequency (high markers) approach the competitor's scent marksmore quickly and spend more time in counter-marking than thosewhich initially invest relatively little (low markers). Ina sib-sib experimental design, simulated presence of predationrisk (urine of ferrets, Mustela putorius furo) caused bothkinds of individual to approach the competitor's marks moreslowly, but high markers approached more quickly than low markersand spent more time in the vicinity of the competitor's marks.Only high markers significantly reduced their overmarking ofthe competitor's scent. These results suggest (1) that thereis a unique danger inherent to scent-marking at high frequenciesand (2) that high-marking males were prepared to accept increasedcosts of intrasexual competition in order to reduce the riskof predation. Further tests using the scent of naked mole-rats, Heterocephalus glaber, showed that these effects were not elicited simply by an unfamiliar odor. We discuss reasons for the observeddifference in response to predation risk between the groups,and the implications of these results for counter-selectionon scent-marking strategies.     

Biologically meaningful scents: a framework for understanding predator–prey research across disciplines

Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information – scents – in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti‐anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory‐based risk discrimination. To understand the highly variable literature in this area, we adopt a multi‐disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time‐limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti‐anxiolytic compounds, and help explain the observed variation in post‐traumatic‐related behaviours (including post‐traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans.     

Mammalian predator scent, vegetation cover and tree seedling predation by meadow voles

Herbivores are thought to respond to the increased risk of attack by predators during foraging activities by concentrating feeding in safe habitats and by reducing feeding in the presence of predators. We tested these hypotheses by comparing tree seedling predation by meadow voles within large outdoor enclosures treated either with scent of large mammalian predators (red fox, bobcat, coyote) or a control scent (vinegar). In addition, we compared the distribution of voles in relation to naturally occurring variation in vegetation cover and the tendency of voles to attack tree seedlings planted in small patches with cover manipulation (intact, reduced or removed cover). Predator scent did not affect the rate or spatial distribution of tree seedling predation by voles, nor did it affect giving up densities (a surrogate of patch quitting harvest rate), survival rates, body size or habitat distribution of voles. In both predator scent and vinegar treatments voles preferred abundant vegetation providing good cover, which was also the site of almost all tree seedling predation. We conclude that large mammalian predator scent does not influence the perception by voles of the general safety of habitat, which is more strongly affected by the presence of cover.     

Antipredatory Response and Food Intake in Wood Mice (Apodemus sylvaticus) under Simulated Predation Risk by Resident and Novel Carnivorous Predators

Chemical signals left by predators are a potential source of information about the risk of predation, and small mammals are known to take them into account when making decisions. We investigated whether wood mice (Apodemus sylvaticus) are more likely to avoid the faeces of resident predators (red fox Vulpes vulpes and common genet Genetta genetta) vs. a novel predator (European pine marten Martes martes). Odour recognition would increase perceived predation risk and reduce food intake by individual mice. Wood mice response to predators was analysed by live‐trapping using two untreated controls (baited/non‐baited) and traps experimentally manipulated with three predator treatments (faeces of red fox, common genet or pine marten). Traps were baited with 4 g of toasted corn, and food intake by wood mice was determined as the amount of bait remaining in each trap. We found that traps treated with faeces of resident predators were the most avoided, and the number of captures in traps treated with pine marten faeces was similar to the control‐baited traps. The variation found in food intake was explained by the interaction between the types of treatment and breeding condition. Food intake was similar in control‐baited traps and in traps with faeces of pine marten, but when predation risk by resident predators (red fox and common genet) was simulated, breeders reduced food intake significantly as compared to non‐breeders. These results indicate that predator recognition and feeding behaviour under predation risk depend on individual factors and the balance of costs‐benefits in each particular predation risk situation at a given place and time.     

Fossils and phylogeny uncover the evolutionary history of a unique antipredator behaviour

Recently, two squirrel species (Spermophilus spp.) were discovered to anoint their bodies with rattlesnake scent as a means of concealing their odour from these chemosensory predators. In this study, we tested multiple species with predator scents (rattlesnake and weasel) to determine the prevalence of scent application across the squirrel phylogeny. We reconstructed the evolutionary history of the behaviour using a phylogenetic analysis and fossil records of historic predator co‐occurrence. Squirrels with historical and current rattlesnake co‐occurrence all applied rattlesnake scent, whereas no relationship existed between weasel scent application and either weasel or rattlesnake co‐occurrence. This was surprising because experimental tests confirmed rattlesnake and weasel scent were both effective at masking prey odour from hunting rattlesnakes (the primary predator of squirrels). Ancestral reconstructions and fossil data suggest predator scent application in squirrels is ancient in origin, arising before co‐occurrences with rattlesnakes or weasels in response to some other, now extinct, chemosensory predator.     

A predator's costs of overcoming the confusion-effect of swarming prey

Swarms of prey are known to have a confusion effect on predators that increases with swarm density. Hungry sticklebacks (Gasterosteus aculeatus) overcome the confusion (Heller & Milinski 1979) except when frightened by a predator of their own (Milinski & Heller 1978). This study investigates whether the costs of overcoming the confusion consist of decreased attention for predators. Hungry sticklebacks detected a predator of their own less often when they fed upon a prey swarm of high density than when they attacked a low density swarm. They also overlooked the predator more frequently when they fed with a high rate than with a low one in the same high density. Thus, there is a cost of attacking high density swarms. These results confirm two necessary conditions of a model for balancing feeding rate and predation risk (Milinski & Heller 1978). The decreased attention is assumed to be due to the limited channel capacity of the nervous system in processing sensory information.     

Adult frogs are sensitive to the predation risks of olfactory communication

Olfaction is a common sensory mode of communication in much of the Vertebrata, although its use by adult frogs remains poorly studied. Being part of an open signalling system, odour cues can be exploited by 'eavesdropping' predators that hunt by smell, making association with odour a high-risk behaviour for prey. Here, we show that adult great barred frogs (Mixophes fasciolatus) are highly attracted to odour cues of conspecifics and those of sympatric striped marsh frogs (Limnodynastes peronii). This attraction decreased significantly with the addition of odours of a scent-hunting predator, the red-bellied black snake (Pseudechis porphyriacus), indicating that frogs perceived predation risks from associating with frog odours. Male frogs, however, maintained some attraction to unfamiliar conspecific scents even with predator odours present, suggesting that they perceived benefits of odour communication despite the risk. Our results indicate that adult frogs can identify species and individuals from their odours and assess the associated predation risk, revealing a complexity in olfactory communication previously unknown in adult anurans.     

Type and nature of cues used by Nucella lapillus to evaluate predation risk

The ability of prey to detect and adequately respond to predation risk influences immediate survival and overall fitness. Chemical cues are commonly used by prey to evaluate risk, and the purpose of this study was to elicit the nature of cues used by prey hunted by generalist predators. Nucella lapillus are common, predatory, intertidal snails that evaluate predatory risk using chemical cues. Using Nucella and a suite of its potential predators as a model system, we explored how (1) predator type, (2) predator diet, and (3) injured conspecifics and heterospecifics influence Nucella behavior. Using laboratory flumes, we determined that Nucella responded only to the invasive green crab (Carcinus maenas), the predator it most frequently encounters. Nucella did not respond to rock crabs (Cancer irroratus) or Jonah crabs (Cancer borealis), which are sympatric predators but do not frequently encounter Nucella because these crabs are primarily subtidal. Predator diet did not affect Nucella responses to risk, although starved predator response was not significantly different from controls. Since green crabs are generalist predators, diet cues do not reflect predation risk, and thus altering behavior as a function of predator diet would not likely benefit Nucella. Nucella did, however, react to injured conspecifics, a strategy that may allow them to recognize threats when predators are difficult to detect. Nucella did not react to injured heterospecifics including mussels (Mytilus edulis) and herbivorous snails Littorina littorea, suggesting that they are responding to chemical cues unique to their species. The nature of cues used by Nucella allows them to minimize costs associated with predator avoidance.     

Antipredatory behaviour in lizards: interactions between group size and predation risk

Group size effects on antipredatory behaviour are well documented in numerous animals, but little is known about how the level of predation risk influences this process. We tested the hypothesis that group size and level of risk interact to affect the levels of antipredatory behaviour in the group-living sun skink, Lampropholis delicata. We controlled the size of lizard groups (N=1, 2, 4, 8 or 12 females) and altered predation risk by providing either a basking tile covered with chemical cues from a predator (high risk) or one without scent (low risk). The time allocated to individual antipredatory behaviour decreased significantly with increasing group size. The relation between group size and time allocated to individual antipredatory behaviour was nonlinear and asymptotic, and did not change under low and high risks of predation. However, group size and predation risk interacted to affect significantly the time that lizards allocated to antipredatory behaviour. When the overall risk from predators was high, individual responsiveness decreased strongly as group size became larger. In contrast, when the overall risk from predators was low, individual responsiveness decreased weakly as group size became larger. Consequently, the time that lizards allocated to antipredatory behaviour under different risks of predation converged as group size increased.