Assess Predation Risk Research Articles

Behavioral response of a generalist predator to chemotactile cues of two taxonomically distinct prey species

Chemotactile cues unintentionally left by animals can play a major role in predator–prey interactions. Specialized predators can use them to find their prey, while prey individuals can assess predation risk. However, little is known to date about the importance of chemotactile cues for generalist predators such as ants. Here, we investigated the response of a generalized predatory ant, Formica polyctena, to cues of two taxonomically distinct prey: a spider (Pisaura mirabilis) and a cricket (Nemobius sylvestris). In analogy, we studied whether crickets and spiders showed antipredator behavior in response to ant cues. When confronted with cues of the two prey species, Formica polyctena workers showed increased residence time and reduced movement speed, which suggests success-motivated searching behavior and thus increased foraging effort. The ants’ response did not differ between cues of the two prey species, coinciding with similar aggression and consumption rates of dead prey. However, the cuticular hydrocarbons, which likely resemble part of the potential cues, differed strongly between the species, with only few methyl-branched alkanes in common. This suggests that ants respond to multiple compounds left by other organisms with prey-search behavior. The two prey species, in turn, showed no detectable antipredator behavior in response to ant cues. Our study shows that ants can detect and respond to chemotactile cues of taxonomically and ecologically distinct prey species, probably to raise their foraging success. Using such chemotactile cues for prey detection may drastically increase their foraging efficiency and thus contribute to the high ecological success of ants.

Only fear the fatal foe: predation risk assessment by eastern newts (Notophthalmus viridescens) in response to common snapping turtles and other potential predators

Many organisms utilize toxic or noxious compounds as a means of deterring predation. Eastern newts (Notopthalmus viridescens), along with other species in the family Salamandridae, possess a potent neurotoxin called tetrodotoxin (TTX). Although TTX can serve as an effective antipredator mechanism in species of newts with high concentrations (e.g., Taricha), eastern newts have relatively low levels of toxicity in comparison to those species, and it may not serve as an effective antipredator mechanism against all threats. In this case, they may benefit rather by utilizing behavioral changes to avoid initial contact with predators. We tested for predator-avoidance behavior in newts by exposing individuals to kairomones from various predators. We recorded activity patterns of newts when they were exposed to cues from potential predators including bullfrogs (Lithobates catesbeiana), water snakes (Nerodia sipedon) and snapping turtles (Chelydra serpentina), as well as a non-predator (bullfrog tadpoles), and a control (deionized water). Newts reduced activity when exposed to snapping turtle stimuli, but did not change activity when exposed to any other chemical cues. We verified that newts interact with this predator by trapping snapping turtles found in ponds from which newts were collected. Finally, we used turtles caught during this sampling to test whether they are an actual predator of newts and whether newts shift microhabitat use when exposed to this predator. In each replicate, turtles consumed newts, and newts spatially avoided the snapping turtle, relative to a control. The results of these experiments indicate newts rely on predator-avoidance behavior to reduce the probability of being consumed by snapping turtles, but do not reduce activity in response to other potential predators that may only consume them rarely.

Predator-risk-sensitive foraging behavior of Carolina chickadees (Poecile carolinensis) and tufted titmice (Baeolophus bicolor) in response to the head orientation of snake predator models

The risk of predation varies with behavioral cues and body characteristics of potential predators. One such body characteristic is the head/face orientation of the predator. However, a prey individual’s ability to detect the head may be more difficult when the predator’s body is serpentine, with little distinguishing the head from the tail. Here, we tested whether individuals in mixed-species flocks of Carolina chickadees (Poecile carolinensis) and tufted titmice (Baeolophus bicolor) distinguish the head orientation of predator snake models. We conducted behavioral observations at multiple sites each having a bird feeder stocked with seed. Each chickadee and titmouse flock was exposed to two counterbalanced trials: a snake model with head closest to the seed area of the feeder and with tail closest to the seed area of the feeder. Observers recorded the number of seeds taken by each species and also the number of unsuccessful feeder visits. Chickadees and, to a lesser extent, titmice took fewer seeds and had more unsuccessful feeder visits when the head of the snake model was closest to the seed, compared to when the tail was closest to the seed. Titmice, furthermore, had more unsuccessful feeder visits to the black snake model type representing a real snake nest predator for these small songbirds. Therefore, head orientation seems an important factor that some species use to assess predation risk, even for predatory species where head orientation may be a subtle cue.

Converting Predation Cues into Conservation Tools: The Effect of Light on Mouse Foraging Behaviour.

Prey face a conflict between acquiring energy and avoiding predators and use both direct and indirect cues to assess predation risk. Illumination, an indirect cue, influences nocturnal rodent foraging behaviour. New Zealand holds no native rodent species but has introduced mice (Mus musculus) that severely impair native biodiversity. We used Giving-Up Densities (GUDs) and observations of foraging frequency and duration to assess if artificial light induces risk avoidance behaviour in mice and could limit their activity. We found both captive (wild strain) mice in outdoor pens and wild mice within a pest fenced sanctuary (Maungatautari, New Zealand) displayed avoidance behaviour in response to illumination. In captivity, total foraging effort was similar across lit and unlit pens but mice displayed a strong preference for removing seeds from dark control areas (mean: 15.33 SD: +/-11.64 per 3.5 hours) over illuminated areas (2.00 +/-3.44). Wild mice also removed fewer seeds from illuminated areas (0.42 +/-1.00 per 12 hours) compared to controls (6.67 +/-9.20). Captive mice spent less than 1.0% of available time at illuminated areas, versus 11.3% at controls; visited the lit areas less than control areas (12.00 +/- 9.77 versus 29.00 +/-21.58 visits respectively); and spent less time per visit at illuminated versus control areas (8.17 +/-7.83 versus 44.83 +/-87.52 seconds per visit respectively). Illumination could provide protection at ecologically sensitive sites, damaged exclusion fences awaiting repair, fence terminus zones of peninsula sanctuaries and shipping docks that service offshore islands. We promote the hypothesis that the tendency of mice to avoid illumination could be a useful conservation tool, and advance knowledge of risk assessment and foraging under perceived danger.

Olfaction: An Overlooked Sensory Modality in Applied Ethology and Animal Welfare.

It has long been known that odors and olfaction play a major role in behavioral development and expression in animals. The sense of smell is employed in numerous contexts, such as foraging, mate choice, and predation risk assessment. Indeed, olfaction is the primary sensory modality for most mammals, and many domestic species kept by humans, including chickens (1). Odors are therefore likely to influence many of the handling and management procedures carried out with animals, whether on farms, in zoos, in the laboratory, or in the family home. Despite this, applied ethologists and animal welfare scientists have not to any great extent investigated chemosensory perception or included odors in their studies.

Parasite and predator risk assessment: nuanced use of olfactory cues.

Foraging herbivores face twin threats of predation and parasite infection, but the risk of predation has received much more attention. We evaluated, experimentally, the role of olfactory cues in predator and parasite risk assessment on the foraging behaviour of a population of marked, free-ranging, red-necked wallabies (Macropus rufogriseus). The wallabies adjusted their behaviour according to these olfactory cues. They foraged less, were more vigilant and spent less time at feeders placed in the vicinity of faeces from dogs that had consumed wallaby or kangaroo meat compared with that of dogs feeding on sheep, rabbit or possum meat. Wallabies also showed a species-specific faecal aversion by consuming less food from feeders contaminated with wallaby faeces compared with sympatric kangaroo faeces, whose gastrointestinal parasite fauna differs from that of the wallabies. Combining both parasite and predation cues in a single field experiment revealed that these risks had an additive effect, rather than the wallabies compromising their response to one risk at the expense of the other.

Social cichlid fish change behaviour in response to a visual predator stimulus, but not the odour of damaged conspecifics

Predation is one of the primary drivers of fitness for prey species. Therefore, there should be strong selection for accurate assessment of predation risk, and whenever possible, individuals should use all available information to fine-tune their response to the current threat of predation. Here, we used a controlled laboratory experiment to assess the responses of individual Neolamprologus pulcher, a social cichlid fish, to a live predator stimulus, to the odour of damaged conspecifics, or to both indicators of predation risk combined. We found that fish in the presence of the visual predator stimulus showed typical antipredator behaviour. Namely, these fish decreased activity and exploration, spent more time seeking shelter, and more time near conspecifics. Surprisingly, there was no effect of the chemical cue alone, and fish showed a reduced response to the combination of the visual predator stimulus and the odour of damaged conspecifics relative to the visual predator stimulus alone. These results demonstrate that N. pulcher adjust their anti-predator behaviour to the information available about current predation risk, and we suggest a possible role for the use of social information in the assessment of predation risk in a cooperatively breeding fish.

Predation Risk Perception, Food Density and Conspecific Cues Shape Foraging Decisions in a Tropical Lizard.

When foraging, animals can maximize their fitness if they are able to tailor their foraging decisions to current environmental conditions. When making foraging decisions, individuals need to assess the benefits of foraging while accounting for the potential risks of being captured by a predator. However, whether and how different factors interact to shape these decisions is not yet well understood, especially in individual foragers. Here we present a standardized set of manipulative field experiments in the form of foraging assays in the tropical lizard Anolis cristatellus in Puerto Rico. We presented male lizards with foraging opportunities to test how the presence of conspecifics, predation-risk perception, the abundance of food, and interactions among these factors determines the outcome of foraging decisions. In Experiment 1, anoles foraged faster when food was scarce and other conspecifics were present near the feeding tray, while they took longer to feed when food was abundant and when no conspecifics were present. These results suggest that foraging decisions in anoles are the result of a complex process in which individuals assess predation risk by using information from conspecific individuals while taking into account food abundance. In Experiment 2, a simulated increase in predation risk (i.e., distance to the feeding tray) confirmed the relevance of risk perception by showing that the use of available perches is strongly correlated with the latency to feed. We found Puerto Rican crested anoles integrate instantaneous ecological information about food abundance, conspecific activity and predation risk, and adjust their foraging behavior accordingly.

Distress Calls of a Fast-Flying Bat (Molossus molossus) Provoke Inspection Flights but Not Cooperative Mobbing.

Many birds and mammals produce distress calls when captured. Bats often approach speakers playing conspecific distress calls, which has led to the hypothesis that bat distress calls promote cooperative mobbing. An alternative explanation is that approaching bats are selfishly assessing predation risk. Previous playback studies on bat distress calls involved species with highly maneuverable flight, capable of making close passes and tight circles around speakers, which can look like mobbing. We broadcast distress calls recorded from the velvety free-tailed bat, Molossus molossus, a fast-flying aerial-hawker with relatively poor maneuverability. Based on their flight behavior, we predicted that, in response to distress call playbacks, M. molossus would make individual passing inspection flights but would not approach in groups or approach within a meter of the distress call source. By recording responses via ultrasonic recording and infrared video, we found that M. molossus, and to a lesser extent Saccopteryx bilineata, made more flight passes during distress call playbacks compared to noise. However, only the more maneuverable S. bilineata made close approaches to the speaker, and we found no evidence of mobbing in groups. Instead, our findings are consistent with the hypothesis that single bats approached distress calls simply to investigate the situation. These results suggest that approaches by bats to distress calls should not suffice as clear evidence for mobbing.

Stream Salamanders Accurately Assess Size-Dependent Predation Threats

Individual size is an important determinant of the outcomes of inter- and intraspecific interactions. Different-sized members of a guild might represent prey, competitors, or predators. Although direct predation rates might be low, trait-mediated indirect effects of predators on prey can yield altered activity, microhabitat use, survival, and growth. If individuals respond to all sizes of a predator regardless of the predation threat, antipredator behaviors might incur costs for prey as they forgo foraging opportunities or experience predation by other predators. Accurate assessment of predation risk would minimize costs resulting from antipredator behavior. We evaluated the ability of larval salamanders to assess predation risk and alter their habitat selection in response to intraguild competitors and predators. Specifically, we assessed behavioral responses to the presence of a conspecific, a similarly sized heterospecific, and a small or large individual of a predatory species. We predicted that larval salamanders would select habitat differently in the presence of a large predatory heterospecific, but not in the presence of similarly sized heterospecifics or conspecifics. The focal species occupied habitat 29 6 0.02% farther from a large heterospecific predator than from small heterospecifics, even if the heterospecifics were smaller individuals of the predatory species. The focal species also exhibited escape behaviors only in the presence of the large members of the predatory species. These data indicate that salamander larvae can assess size-specific predation threats, minimizing predation risk through use of antipredator behaviors.

Chemosensory Perception of Predators by Larval Amphibians Depends on Water Quality.

The acquisition of sensory information by animals is central to species interactions. In aquatic environments, most taxa use chemical cues to assess predation risk and other key ecological factors. A number of laboratory studies suggest that anthropogenic pollutants can disrupt chemoreception, even when at low, non-toxic concentrations, but there are few tests of whether real-world variation in water quality affects chemoreception. Here we investigate whether chemosensory perception of predators by the gray treefrog, Hyla versicolor, depends on water quality. We evaluated the anti-predator response of anuran tadpoles housed in water collected from three sites that represent strong contrasts in the concentration and types of dissolved solids: de-chlorinated tap water, water from an impaired stream, and treated wastewater effluent. Behavioral assays were conducted in laboratory aquaria. Chemical cues associated with predation were generated by feeding tadpoles to dragonfly predators held in containers, and then transferring aliquots of water from dragonfly containers to experimental aquaria. Tadpoles housed in tap water responded to predator cues with an activity reduction of 49%. Tadpoles housed in stream water and wastewater effluent responded to predator cues by reducing activity by 29% and 24% respectively. The results of factorial ANOVA support the hypothesis that the response to predator cues depended on water type. These results show that alteration of the chemical environment can mediate chemical perception of predators in aquatic ecosystems. Because most aquatic species rely on chemoreception to gather information on the location of food and predators, any impairment of sensory perception likely has important ecological consequences.

Assessment of predation risk through referential communication in incubating birds.

Parents of many bird species produce alarm calls when they approach and deter a nest predator in order to defend their offspring. Alarm calls have been shown to warn nestlings about predatory threats, but parents also face a similar risk of predation when incubating eggs in their nests. Here, I show that incubating female Japanese great tits, Parus minor, assess predation risk by conspecific alarm calls given outside the nest cavity. Tits produce acoustically discrete alarm calls for different nest predators: “jar” calls for snakes and “chicka” calls for other predators such as crows and martens. Playback experiments revealed that incubating females responded to “jar” calls by leaving their nest, whereas they responded to “chicka” calls by looking out of the nest entrance. Since snakes invade the nest cavity, escaping from the nest helps females avoid snake predation. In contrast, “chicka” calls are used for a variety of predator types, and therefore, looking out of the nest entrance helps females gather information about the type and location of approaching predators. These results show that incubating females derive information about predator type from different types of alarm calls, providing a novel example of functionally referential communication.

Anti‐predator behaviour in a procellariid seabird: Wedge‐tailed shearwaters do not respond to the odour of introduced ship rats

AbstractSeabirds are particularly vulnerable to introduced alien mammalian predators, especially invasive rats, which are the main contributors to seabird extinction and endangerment in many places worldwide. However, this appears context‐dependent because, paradoxically, cases of apparent long‐term coexistence between rats and some species of seabird have been reported for centuries, in various locations. Among seabirds, procellariiforms are known to have developed a range of olfactory‐driven behaviours, such as partner recognition and homing. Olfaction could be an effective means of recognizing and thereafter avoiding invasive predators. However, the role of olfaction in predation risk assessment has not yet been examined in any procellariiform. Here, we investigated, through a Y‐maze experiment, whether the wedge‐tailed shearwater (Puffinus pacificus) avoided the odour of one of the most damaging alien predators on islands, the ship rat (Rattus rattus). The experiment was conducted in different ecological contexts on three neighbouring islets off New Caledonia having different communities of invasive rats. Contrary to our expectations, the wedge‐tailed shearwater either did not detect or did not avoid the odour of the ship rat, despite about 175 years of coexistence between rats and shearwaters in New Caledonia. These findings highlight the need for further investigations (across species, across sites) into the factors underpinning the paradox between high vulnerability and the surprising long‐term coexistence between procellariid seabirds and alien invasive rats.

Algal Turbidity Reduces Risk Assessment Ability of the Three‐Spined Stickleback

AbstractRecent anthropogenic increases in algal turbidity in aquatic habitats have been suggested to affect the ability of fish to assess predation risk. We investigated the response of feeding three‐spined sticklebacks (Gasterosteus aculeatus) exposed to a sudden appearance of an avian predator (the silhouette of common tern, Sterna hirundo), under clear and turbid water conditions. As stickleback use social cues to aid in predator avoidance, we also tested whether turbidity affected social information use by manipulating group size. We found that in turbid water, a smaller proportion of fish would escape from the feeding area, that the distance escaped was shorter and that a smaller proportion of fish fled into shelter. Larger group size was associated with longer escape distance and greater shelter use. However, there was no effect of group size on the proportion of fish that escaped the arena. The effect of group size was similar for turbid and clear water. Our finding that the fish showed a weaker antipredator response suggests that turbidity impedes their risk assessment capability. However, the sticklebacks were still able to benefit of the social facilitation provided by being in a group. This suggests that algal turbidity has detrimental effects on the ability of sticklebacks to assess predation risk from avian predators in shallow water. An implication is that in shallow water fish may be more vulnerable to avian predation under turbid conditions.

Evidence that the house finch (Carpodacus mexicanus) uses scent to avoid omnivore mammals

The detection of predator chemical cues is an important antipredatory behaviour as it allows an early assessment of predation risk without encountering the predator and therefore increases survival. For instance, since chemical cues are often by-products of metabolism, olfaction may gather information not only on the identity but also about the diet of predators in the vicinity. Knowledge of the role of olfaction in the interactions of birds with their environment, in contexts as important as predator avoidance, is still scarce. We conducted two two-choice experiments to explore 1) whether the house finch Carpodacus mexicanus can detect the chemical cues of a marsupial predatory mammal, the common opossum (Didelphis marsupialis), and 2) whether its response to such cues is influenced by the recent diet of this omnivorous predator, as this would increase the accuracy with which the risk of predation is assessed. House finches avoided the area of the apparatus containing the scent of the predator, and this effect did not depend on the recent diet (bait used to lace the traps) of the predator. Our results provide clear evidence that house finches detect and use the chemical cues of predators to assess the level of predation risk of an area and avoid it.

I smell a rat: Can New Zealand birds recognize the odor of an invasive mammalian predator?

Abstract Although it is well known that birds can assess predation risk through visual and auditory cues, there has been little research into whether similar processes occur with olfactory cues. We examined the role of odor cues in assessing nest predation risk in four species of passerine birds in New Zealand. We compared the ability of two introduced European species (common starling Sturnus vulgaris and song thrush Turdus philomelos) and two native New Zealand species (rifleman Acanthisitta chloris and South Island robin Petroica australis) to respond to the scent of rat urine placed in the nest. Rats are an introduced predator in New Zealand and we expected the native birds, which did not co-evolve with any mammalian predators, to lack behavioral adaptations to the scent of rats at their nest. As expected, both riflemen and robins failed to show any change in their behavior at their nest when rat urine was present compared to a control period in which no scent was present. However, a similar lack of response was observed in the introduced song thrush; only the common starling changed its behavior in the presence of the rat urine. Starlings with rat urine at the nest box were more likely to hesitate before entering and they also approached the nest, but refused to enter more often in the presence of rat scent. Both responses suggest they detected the presence of a predator and changed their behavior to minimize risk to themselves. Although based on a small number of species, our results suggest that responses to predator scent may be less common in New Zealand species, and may be a factor contributing to the vulnerability of native birds to introduced mammalian predators.

Do changes in reef habitats influence relative predation risk on the juvenile Australasian spiny lobster, Jasus edwardsii (Hutton, 1875)?

Kelp habitats are in decline in many temperate coastal regions of the world due to climate change and expansion of populations of grazing urchins. The loss of kelp habitat may influence the vulnerability to predators of the juveniles of commercially important species. In this study relative predation rates for kelp versus barren reef habitat were measured for early juvenile Australasian spiny lobster, Jasus edwardsii (Hutton, 1875), on the northeastern coast of New Zealand using tethering methods. Variation in assemblages of predators over small spatial scales appeared to be more important for determining the relative predation of lobsters, regardless of habitat type. Therefore, the assessment of relative predation risk to early juvenile lobsters between kelp and barren habitats will require more extensive sampling at a small spatial scale, as well as a specific focus on sampling during crepuscular and nocturnal periods when these lobsters are most at risk of predation.

Nonconsumptive Effects of Predation and Impaired Chemosensory Risk Assessment on an Aquatic Prey Species

Weak levels of acidity impair chemosensory risk assessment by aquatic species which may result in increased predator mortalities in the absence of compensatory avoidance mechanisms. Using replicate populations of wild juvenile Atlantic salmon (Salmo salar) in neutral and acidic streams, we conducted a series of observational studies and experiments to identify differences in behaviours that may compensate for the loss of chemosensory information on predation risk. Comparing the behavioural strategies of fish between neutral and acidic streams may elucidate the influence of environmental degradation on nonconsumptive effects (NCEs) of predation. Salmon in acidic streams are more active during the day than their counterparts in neutral streams, and are more likely to avoid occupying territories offering fewer physical refugia from predators. Captive cross-population transplant experiments indicate that at equal densities, salmon in acidic streams do not demonstrate relative decreases in growth rate as a result of their different behavioural strategies. Instead, altering diel activity patterns to maximize visual information use and occupying relatively safer territories appear sufficient to offset increased predation risk in acidic streams. Additional strategies such as elevated foraging rates during active periods or adopting riskier foraging tactics are necessary to account for the observed similarities in growth rates.

Strong food odours mask predation risk and affect evocation of defence behaviours in the tadpoles of Sphaerotheca breviceps

Tadpoles of Sphaerotheca breviceps detect food and predators using waterborne chemical cues (odours), which evoke appropriate behaviour. The present study aimed to determine whether they are capable of resolving the conflict between foraging choice and predator avoidance on encountering both food and predatory chemical cues together. Experiments were designed using an association choice apparatus in which prey tadpoles were given a choice to move themselves close to or away from a given stimulus (food or a predator). Food odours were either strong or weak. Tadpoles of Hoplobatrachus tigerinus (n = 4) were placed in an open-ended mesh cage wrapped in a cheese cloth that provided predator cues. The time spent by the test tadpoles in the predator’s zone or away from it and the time spent feeding were recorded for 10 min (n = 25 trials). When food odours were weak, the prey tadpoles avoided predators and spent significantly more time in the predator-free zone. In contrast, when food odours were strong, they foraged equally in the two zones of the test apparatus regardless of the presence or absence of predators. These findings confirm the inherent ability of S. breviceps tadpoles to distinguish between food and predators, and indicate that strong food odours mask predation risk. We suggest that foraging theory and the predation risk allocation hypothesis should include factors that mislead prey during predation risk assessment and the evocation of defence behaviours.

Temporal constraints on predation risk assessment in a changing world

Habitat degradation takes various forms and likely represents the most significant threat to our global biodiversity. Recently, we have seen considerable attention paid to increasing global CO2 emissions which lead to ocean acidification (OA). Other stressors, such as changing levels of ultraviolet radiation (UVR), also impact biodiversity but have received much less attention in the recent past. Here we examine fundamental questions about temporal aspects of risk assessment by coral reef damselfish and provide critical insights into how OA and UVR influence this assessment. Chemical cues released during a predator attack provide a rich source of information that other prey animals use to mediate their risk of predation and are the basis of the majority of trait-mediated indirect interactions in aquatic communities. However, we have surprisingly limited information about temporal aspects of risk assessment because we lack knowledge about how long chemical cues persist after they are released into the environment. Here, we showed that under ambient CO2 conditions (~385μatm), alarm cues of ambon damselfish (Pomacentrus amboinensis) did not degrade within 30min in the absence of ultraviolet radiation (UVR), but were degraded within 15min when the CO2 was increased to ~905μatm. In experiments that used filters to eliminate UVR, we found minimal degradation of alarm cues within 30min, whereas under ambient UVR conditions, alarm cues were completely degraded within 15min. Moreover, in the presence of both UVR and elevated CO2, alarm cues were broken down within 5min. Our results highlight that alarm cues degrade surprisingly quickly under natural conditions and that anthropogenic changes have the potential to dramatically change rates of cue degradation in the wild. This has considerable implications for risk assessment and consequently the importance of trait-mediated indirect interactions in coral-reef communities.