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

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

Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories

Abstract Predation is recognized as a major selective pressure influencing population dynamics and evolutionary processes. Prey species have developed a variety of predator avoidance strategies, not least of which is olfactory recognition. However, within Australia, European settlement has brought with it a number of introduced predators, perhaps most notably the red fox (Vulpes vulpes) and domestic cat (Felis catus), which native prey species may be unable to recognize and thus avoid due to a lack of coexistence history. This study examined the response of native Tasmanian swamp rats (Rattus lutreolus velutinus) to predators of different coexistence history (native predator‐ spotted‐tail quoll (Dasyurus maculatus), domestic cats and the recently introduced red fox). We used an aggregate behavioural response of R. l. velutinus to predator integumental odour in order to assess an overall behavioural response to predation risk. Rattus lutreolus velutinus recognized the integumental odour of the native quoll (compared with control odours) but did not respond to either cat or fox scent (compared with control odur). In contrast, analyses of singular behaviours resulted in the conclusion that rats did not respond differentially to either native or introduced predators, as other studies have concluded. Therefore, measuring risk assessment behaviours at the level of overall aggregate response may be more beneficial in understanding and analysing complex behavioural patterns such as predator detection and recognition. These results suggest that fox and cat introductions (and their interactive effects) may have detrimental impacts upon small native Tasmanian mammals due to lack of recognition and thus appropriate responses.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Habitat but not group size or recent predator activity affect corvid collective vigilance at carcasses

Vigilance is an important anti-predator behaviour that can be an indicator of the predation risk faced by potential prey animals. Here, we assess the collective vigilance, or the vigilance level of an entire group, of corvids (Family: Corvidae) at experimentally placed carcasses in a desert environment in Australia. Specifically, we explore the relationship between collective vigilance levels and the habitat in which the carcass was placed, the time since a potential predator (dingo Canis dingo, wedge-tailed eagle Aquila audax or red fox Vulpes vulpes) was present at a carcass, and the group size of corvids around the carcass. We found that corvids are more vigilant in open habitat, but that group size and the recent presence of a potential predator does not affect the collective vigilance behaviour of corvids. The results demonstrate the important link between habitat and vigilance, and that animals may adopt anti-predator behaviours irrespective of the size of the group in which they occur or the recent presence of a potential predator.     

Linking Morphological and Behavioural Defences: Prey Fish Detect the Morphology of Conspecifics in the Odour Signature of their Predators

Predation is a strong selective force acting on both morphology and behaviour of prey animals. While morphological defences (e.g. crypsis, presence of armours or spines or specific body morphologies) and antipredator behaviours (e.g. change in foraging or reproductive effort, or hiding and fleeing behaviours) have been widely studied separately, few studies have considered the interplay between the two. The question raised in our study is whether antipredator behaviours of a prey fish to predator odours could be influenced by the morphology of prey conspecifics in the diet of the predator. We used goldfish (Carassius auratus) as our test species; goldfish exposed to predation risk significantly increase their body depth to length ratio, which gives them a survival advantage against gape‐limited predators. We exposed shallow‐bodied and deep‐bodied goldfish to the odour of pike (Esox lucius) fed either form of goldfish. Deep‐bodied goldfish displayed lower intensity antipredator responses than shallow‐bodied ones, consistent with the hypothesis that individuals with morphological defences should exhibit less behavioural modification than those lacking such defences. Moreover, both shallow‐ and deep‐bodied goldfish displayed their strongest antipredator responses when exposed to the odour of pike fed conspecifics of their own morphology, indicating that goldfish are able to differentiate the morphology of conspecifics through predator diet cues. For a given individual, predator threat increases as the prey become more like the individual eaten, revealing a surprising level of sophistication of chemosensory assessment by prey fish.     

Do Australian small mammals respond to native and introduced predator odours?

Abstract Coevolution is thought to have led to many small mammal species avoiding the scent marks of their main mammalian predators, as they provide a reliable cue to predation risk. Most support for this hypothesis comes from northern hemisphere predator/prey systems, however, it is unclear whether this avoidance of predator faecal odour occurs in Australia's mammalian fauna, which has evolved in relative isolation from the rest of the world, and is dominated by marsupials rather than placentals. We tested this theory for an Australian system with marsupial and placental predators and prey, that share a long‐term (>1 million years) or short‐term (<150 years) exposure to each other. The predators were the native marsupial tiger quoll Dasyurus maculatus and the introduced placental red fox Vulpes vulpes. The potential prey were three native rodent species, the bush rat Rattus fuscipes, the swamp rat Rattus lutreolus, the eastern chestnut mouse Pseudomys gracilicaudatus, and the marsupial brown antechinus Antechinus stuartii. Small mammals were captured in Elliott traps with 1/3 of traps treated with fox faeces, 1/3 treated with quoll faeces and the remainder left untreated. The native rodent species all showed avoidance of both tiger quoll and red fox odours whereas the marsupial antechinus showed no responses to either odour. Either predator odour avoidance has not evolved in this marsupial or their reaction to predator odours may be exhibited in ways which are not recognizable through trapping. The avoidance by the rodents of fox odour as well as quoll odour indicates this response may either be due to common components in fox and quoll odour, or it may be a recently evolved response.     

Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.     

Do house mice modify their foraging behaviour in response to predator odours and habitat?

Predator odours and habitat structure are thought to influence the behaviour of small mammalian prey, which use them as cues to reduce risks of predation. We tested this general hypothesis for house mice, Mus domesticus, by manipulating fox odour density via addition of fox scats and habitat via patchy mowing of vegetation, for populations in 15 × 15-m field enclosures. Using giving-up densities (GUDs), the density of food remaining when an animal quits harvesting a patch, we measured foraging behaviours in response to these treatments. Mice consistently avoided open areas, leaving GUDs two to four times greater in these areas than in densely vegetated patches. However, mouse GUDs did not change in response to the addition of fox scats, even immediately after fresh scats were added. There was no interaction between fox odour and habitat use. We then tested whether habituation to fox odours had occurred, by comparing the individual responses to scats of eight mice born into enclosures with fox scats to those of eight mice born into scat-free enclosures and five wild mice. In smaller enclosures, GUDs of trays with scats did not differ from GUDs of trays without scats for any treatment. We conclude that exposure to high levels of fox odours did not alter the foraging behaviour of mice, but that mice did reduce foraging in areas where habitat was removed, perceiving predation risk to be greater in these areas than controls. We suggest further that studies using the ‘scat-at-trap’ technique, which have shown avoidance of predator odours by mice and other small mammals, may overestimate the general avoidance of predator odours by free-living prey, which must forage with a constant background of predator odours.     

Predator naïve minnows respond to their conspecific alarm substance but not the odour from a non-native predator

When exposed to predator cues, ostariophysan fishes exhibit short-term anti-predator behavioural responses in order to minimise predation risk. Non-native predator cues are, however, likely to elicit poor behavioural responses in native prey fishes. This study investigated whether chubbyhead barb Enteromius anoplus, a native freshwater minnow in South Africa, had the innate ability to recognise and respond to largemouth bass Micropterus salmoides, a non-native piscivore. This was experimentally evaluated by investigating behavioural responses to both the non-native predator's odour and damage-released conspecific alarm substance (CAS). Chubbyhead barbs did not exhibit any behavioural response to largemouth bass odour both before and after exposure to CAS. This suggests that the chubbyhead barbs likely lacked the innate ability to recognise the non-native largemouth bass predator kairomones. By comparison, exposure to CAS was associated with significant behavioural responses, with chubbyhead barbs shifting from free-swimming to hovering, and frequent use of refugia. This suggests that despite ineffective response to non-native largemouth bass odour, chubbyhead barbs responded to general predator attack. Overall, this study suggests the potential for non-native largemouth bass to induce negative consumptive effects on chubbyhead barbs due to their inability to identify non-native predator's odour. In addition, nonconsumptive effects are likely due to altered activities in response to predator attack.     

Corticosterone,Avoidance of Novelty,Risk‐Taking and Aggression in a Wild Bird: No Evidence for Pleiotropic Effects

Certain inherent characteristics of individuals can determine both physiological and behavioural responses to environmental challenges, which could drive a correlation between levels of corticosterone (CORT), the most important stress hormone and behavioural profiles. Therefore, CORT level may mediate consistent behaviours along the shy/bold continuum, and thus, it could serve as a pleiotropic basis for behavioural syndromes. Moreover, behavioural responses to environmental challenges may have consequences for CORT concentrations, which would also result in a correlation between physiology and behaviours even without requiring pleiotropic mechanisms. Accordingly, we investigated the relationship between CORT and behaviour in free‐living male collared flycatchers, Ficedula albicollis, using recently developed field assays. More specifically, we characterised novel object avoidance, intraspecific aggression and risk‐taking in males and related these correlated behaviours to the concentration of CORT metabolites in droppings measured by enzyme immunoassay. Individuals with higher levels of excreted CORT metabolites had no consistently higher or lower behavioural scores along the shy/bold spectrum, as avoidance of novelty, aggression and risk‐taking were not systematically related to CORT metabolite concentrations in the same direction. Moreover, environmental challenges owing to the presence of a novel object, territorial intruder and a potential predator caused no elevation in the level of CORT metabolites. Therefore, we did not find correlative evidence for CORT driving correlated behaviours through pleiotropic effects or for particular behaviours during courtship causing elevation in CORT levels.     

The influence of American mink odour on the spatial distribution and behaviour of water voles

The perception and assessment of predation risk often cause changes in the activities of animals and induce behavioural responses that may in turn affect their movements and distribution. To simulate high predation risk in a midfield pond riparian habitat, we used fresh faeces from ranch American mink Neovison vison and recorded behavioural responses of water voles Arvicola amphibius. In areas where mink odour was deployed, the numbers of captured vole individuals and their trappability were significantly lower than in control areas. Several voles migrated from the zones with deployed mink faeces to the areas without faeces, thus proving that increased predation risk affects the distribution of individuals in a population. The response to mink odour was much more pronounced in females than in males; in areas with deployed mink faeces, not a single female was trapped. We conclude that although American mink is a non‐native, invasive predator, water voles respond to mink odour by reducing their activity and/or by avoiding places with higher predation risk.     

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

In natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Bia?owie?a Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.     

First Documentation of Cultural Transmission of Predator Recognition by Larval Amphibians

Predation is a pervasive selective agent shaping a prey's behaviour, morphology and life history. To survive, prey animals have to respond adaptively to predation threats and this can be achieved through learned predator recognition. Cultural transmission of predator recognition is likely a widespread means of learning in social animals, including mammals, birds and fishes. However, no studies have investigated the cultural transmission of predator recognition in amphibians. In our study, we examined whether naïve woodfrog (Rana sylvatica) tadpoles can acquire the recognition of the odour of a predatory tiger salamander (Ambystoma tigrinum) from experienced conspecifics. After conditioning some tutors to recognize salamander odour, we paired naïve observer tadpoles with either a salamander‐naïve or salamander‐experienced tutor and exposed the pairs to either salamander odour or a water control. Observers were subsequently tested alone for a response to salamander odour. We found that when given salamander odour, observer tadpoles that were paired with a salamander‐experienced tutor successfully learned to recognize the salamander odour as a threat, whereas the observers paired with salamander‐naïve tutors did not. Likewise, tadpoles exposed to the water control did not learn to recognize the salamander regardless of whether they were paired with a naïve or experienced tutor. This is the first study demonstrating cultural transmission of predator recognition in an amphibian species.     

Responses of small mammals to Red fox (Vulpes vulpes) odour

This paper describes the responses of three species of rodents (Apodemus sylvaticus, Microtus agrestis and Clethrionomys glareolus) and a shrew (Sore.x araneus) to traps tainted with the faecal odour of a predator, the Red fox. The rodents generally avoided traps bearing fox odour, but readily entered traps marked with rodent odour, whereas shrews entered all traps equally. Among the rodents, avoidance of fox odour was strongest in male A. sylvaticus and C. glareolus and least in M. agrestis and female A. sylvaticus . Fox droppings were found principally along paths and in open habitats where, of the rodents mentioned, they were most likely to be encountered by A. sylvaticus . It was suggested that avoidance of fox faecal and urinary odours in this species, especially by the active males, would reduce the time spent in areas frequented by foxes, and hence reduce the chance of encountering the predator itself. In contrast, M. agresis would seldom encounter fox droppings in its sub-surface runways, so avoidance of fox faecal odour would do little to reduce its chance of encountering the predator. Avoidance by the rodents of the faecal odour of badger, a predator not present in the study areas, was only slightly less marked than their avoidance of fox faecal odour. It was postulated that similar chemicals eliciting avoidance in rodents may commonly occur in the faeces and urine of carnivores.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

Predator occurrence and perceived predation risk determine grouping behavior in guanaco (Lama guanicoe)

Grouping behavior of social ungulates may depend on both predator occurrence and perceived predation risk associated with habitat structure, reproductive state, and density of conspecifics. Over 3 years, we studied grouping behavior of guanaco (Lama guanicoe) families in Chilean Patagonia during the birthing season and determined their response to variation in predator occurrence and perceived predation risk (habitat structure, calf/adult rate, and density of conspecifics). We considered the effect of two predators, puma (Puma concolor) and culpeo fox (Lycalopex culpaeus). We measured two common (family group size and vigilance) and one novel (family group cohesion) behavioral responses of guanaco. Our results show that guanaco family groups adapted their grouping behavior to both predator occurrence and perceived predation risk. Larger family groups were found in open habitats and areas with high puma occurrence, while guanacos stayed in small family groups in areas with high shrub cover or low visibility. Group cohesion increased in areas with higher occurrence of pumas and culpeo foxes, and also increased in smaller family groups and in areas with low guanaco density. Vigilance (number of vigilant adults) was mainly related to group size and visibility, increasing in areas with low visibility, while residual vigilance (vigilance after removing the group‐size effect) did not vary with the explanatory variables examined. Our results suggest that a mix of predator occurrence and perceived predation risk influences guanaco grouping behavior and highlights the importance of evaluating different antipredator responses together and considering all predator species in studies aimed at understanding ungulate behavior.     

Predator odour per se does not frighten domestic horses

Horses frequently react nervously when passing animal production farms and other places with distinctive smells, leading riders to believe that horses are innately frightened by certain odours. In three experiments, we investigated how horses respond to (1) urine from wolves and lions, (2) blood from slaughtered conspecifics and fur-derived wolf odour, and (3) a sudden auditory stimulus in either presence or absence of fur-derived wolf odour. The experiments were carried out under standardised conditions using a total of 45 naïve, 2-year-old horses. In the first two experiments we found that horses showed significant changes in behaviour (Experiments 1 and 2: increased sniffing; Experiment 2 only: increased vigilance, decreased eating, and more behavioural shifts), but no increase in heart rate compared to controls when exposed to predator odours and conspecific blood in a known test environment. However, the third experiment showed that exposure to a combination of wolf odour and a sudden stimulus (sound of a moving plastic bag) caused significantly increased heart rate responses and a tendency to a longer latency to resume feeding, compared to control horses exposed to the sudden stimulus without the wolf odour. The results indicate that predator odour per se does not frighten horses but it may cause an increased level of vigilance. The presence of predator odour may, however, cause an increased heart rate response if horses are presented to an additional fear-eliciting stimulus. This strategy may be adaptive in the wild where equids share habitats with their predators, and have to trade-off time and energy spent on anti-predation responses against time allocated to essential non-defensive activities.     

Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species

Abstract 1. It has become apparent that predators may strongly decrease prey fitness without direct contact with the prey, as they induce the development of defence systems that limit the availability of energy for growth and reproduction. Recent studies suggest that stress proteins may help prey organisms deal with this stress. The pattern is not general, however, and little is known about species differences in physiological traits in coping with predator stress, and covariation of physiological with other antipredator traits. 2. To explore these issues, we quantified levels of constitutive and fish‐induced stress proteins (Hsp60 and Hsp70) and anti‐predator behaviours in larvae of two damselfly species that differ in lifestyle. Both stress proteins were fixed at higher levels in Erythromma najas, which has a slow lifestyle, than in Lestes sponsa, which has a fast lifestyle. Similarly, anti‐predator behaviours were fixed at safer levels in E. najas than in L. sponsa. 3. These results suggest that stress proteins may be part of anti‐predator syndromes of damselfly larvae, and there may be trait co‐specialisation between stress proteins and behavioural anti‐predator traits. Studies formally testing these hypotheses in more species may prove rewarding in advancing our understanding of the functional integration of physiological anti‐predator traits in relation to the prey’s lifestyle.     

Vigilance and grouping in the southern African ground squirrel (Xerus inauris)

Animals may form groups in response to the foraging–vigilance trade‐off, through enhanced predator detection (collective detection hypothesis) or reduced predation risk to the individual (dilution hypothesis), allowing individuals to decrease vigilance levels. Both hypotheses predict decreasing individual vigilance levels with increasing group size; however, the collective detection hypothesis also predicts increasing overall group vigilance with increasing group size. However, in species in which vigilance and foraging are not mutually exclusive, where vigilance may not be as costly, neither of these hypotheses may apply. Here, we examine the relationship between group size and vigilance in the social Cape ground squirrel (Xerus inauris), a species that can combine foraging and vigilance behaviours. Ten groups were observed using scan sampling, measuring both group and individual vigilance and group size. A negative relationship existed between individual vigilance and group size and a positive relationship between group vigilance and group size. Therefore, in Cape ground squirrels, vigilance seems to be costly even though it can be combined with foraging behaviours. Furthermore, group vigilance behaviour gives support to the collective detection hypothesis, whilst individual vigilance gives support to both hypotheses.