Designing anti-predator training to maximize learning and efficacy assessments

Despite the growing need to use conservation breeding and translocations in species’ recovery, many attempts to reintroduce animals to the wild fail due to predation post-release. Released animals often lack appropriate behaviours for survival, including anti-predator responses. Anti-predator training—a method for encouraging animals to exhibit wariness and defensive responses to predators—has been used to help address this challenge with varying degrees of success. The efficacy of anti-predator training hinges on animals learning to recognize and respond to predators, but learning is rarely assessed, or interventions miss key experimental controls to document learning. An accurate measure of learning serves as a diagnostic tool for improving training if it otherwise fails to reduce predation. Here we present an experimental framework for designing anti-predator training that incorporates suitable controls to infer predator-specific learning and illustrate their use with the critically endangered Hawaiian crow, ‘alalā (Corvus hawaiiensis). We conducted anti-predator training within a conservation breeding facility to increase anti-predator behaviour towards a natural predator, the Hawaiian hawk, ‘io (Buteo solitaries). In addition to running live-predator training trials, we included two control groups, aimed at determining if responses could otherwise be due to accumulated stress and agitation, or to generalized increases in fear of movement. We found that without these control groups we may have wrongly concluded that predator-specific learning occurred. Additionally, despite generations in human care that can erode anti-predator responses, ‘alalā showed unexpectedly high levels of predatory wariness during baseline assessments. We discuss the implications of a learning-focused approach to training for managing endangered species that require improved behavioural competence for dealing with predatory threats, and the importance of understanding learning mechanisms in diagnosing behavioural problems.

Anti-predator behaviour of Rhinella major (Müller and Hellmich 1936), with insights into the Rhinella granulosa group

In anurans, the different types of anti-predator behaviour have been documented in isolation, but some species have shown synergistic strategies in different situations. The display of these types of behaviour may be related to the types of predators in the habitat, which boost defensive responses in their prey. However, most reports are mostly opportunistic and punctual observations, not systematic. Here, we report the occurrence of anti-predator behaviour in the toad Rhinella major (Müller and Hellmich 1936) (Amphibia, Anura, Bufonidae) in the face of different handling modes. Probably the disturbance caused by handling had elicited a predator deterrence response in the individual, causing it to rapidly exhibit such behaviour. These conditions are discussed along with an overview of anti-predator behaviour in species of the R. granulosa group and we re-interpreted these strategies for two species in the group.

Urban-nesting mountain chickadees have a reduced response to a simulated predator

Anti-predator behaviour is common among birds, but little research exists on whether differences in the predator landscape between urban and rural habitats results in differential anti-predator behaviour. We compared nest-defence behaviour of mountain chickadees (Poecile gambeli) in urban and rural habitats in Kamloops, BC, Canada to a simulated predator model (snake) on top of nest boxes while incubating females were away from nests on foraging bouts. Upon their return, we recorded proximity to the predator model, latency to contact the nest box and enter the nest, and number of gargle and chick-a-dee calls as measures of anti-predator behaviour and compared multivariate “predator aversion scores” across birds occupying either rural or urban landscapes. Rural-nesting birds had more aversive reactions to the predator model than the urban-nesting birds, which may suggest differences in perceived threat of the model, in combination with increased boldness associated with urban-nesting birds.

Risk-taking behaviour as a central concept in evolutionary biology

Predation is a common cause of mortality, having resulted in the evolution of a diverse kind of anti-predator behaviour across the animal kingdom. One such key behaviour is flight initiation distance (FID), defined as the distance at which animals take flight, when approached by a potential predator such as a human. Extensive research during the past two decades has revealed that optimal anti-predator behaviour is adjusted to life history (the combination of timing of reproduction, fecundity, survivorship, and others). FID is heritable, responds to natural selection and hence shows rapid micro-evolutionary change when animals are exposed to domestication, climate warming, or when introduced to novel environments. Peri-personal space (PPS) and inter-personal space (IPS) may be linked to FID, opening up the possibility of studying these disparate components of behaviour in a common context. Here, I provide a brief review of the extensive literature on FID, but much less well-studied PPS and IPS, and suggest ways in which such behaviour can provide insights into the evolution of anti-predator behaviour and life history. Such knowledge may help us resolve problems in conservation, effects of human disturbance on wild animals, problems of anti-predator behaviour for animal welfare, and potentially even maladaptive anti-predator behaviour and PPS and IPS in humans.

Hide-and-seek strategies and post-contact immobility

To understand why an animal might gain by playing dead, or more precisely, exhibit post-contact immobility (PCI), we consider the context in which this behaviour occurs. Is it, for example, a method by which a potential victim encourages a predator to direct its attention elsewhere? We investigate this possibility by using the marginal value theorem to analyse predator behaviour in the context of this defence strategy by potential prey. We consider two models. In the first, (random revisiting) the predator may return to sites it has already depleted within the patch. In the second, (systematic search) the predator goes only to new sites within the patch. The results of the two models are qualitatively extremely similar. We show that when prey occur in patches, PCI favours prey survival. Indeed, certain antlion larvae have PCI durations characterized by very long half-lives. These appear to be of such long durations that further increases would convey no substantial benefits in redirecting potential predators to other antlions within the patch and subsequently to other patches.

Anti-predator behaviour depends on male weapon size

Tonic immobility and escape are adaptive anti-predator tactics used by many animals. Escape requires movement, whereas tonic immobility does not. If anti-predator tactics relate to weapon size, males with larger weapons may adopt tonic immobility, whereas males with smaller weapons may adopt escape. However, no study has investigated the relationship between weapon size and anti-predator tactics. In this study, we investigated the relationship between male weapon size and tonic immobility in the beetle Gnathocerus cornutus . The results showed that tonic immobility was more frequent in males with larger weapons. Although most studies of tonic immobility in beetles have focused on the duration, rather than the frequency, tonic immobility duration was not affected by weapon size in G . cornutus . Therefore, this study is the first, to our knowledge, to suggest that the male weapon trait affects anti-predator tactics.

Condition-dependent responses of fish to motorboats

Anthropogenic noise is a pollutant of global concern that has been shown to have a wide range of detrimental effects on multiple taxa. However, most noise studies to-date consider only overall population means, ignoring the potential for intraspecific variation in responses. Here, we used field experiments on Australia's Great Barrier Reef to assess condition-dependent responses of blue-green damselfish ( Chromis viridis ) to real motorboats. Despite finding no effect of motorboats on a physiological measure (opercular beat rate; OBR), we found a condition-dependent effect on anti-predator behaviour. In ambient conditions, startle responses to a looming stimulus were equivalent for relatively poor- and good-condition fish, but when motorboats were passing, poorer-condition fish startled at significantly shorter distances to the looming stimulus than better-condition fish. This greater susceptibility to motorboats in poorer-condition fish may be the result of generally more elevated stress levels, as poorer-condition fish had a higher pre-testing OBR than those in better condition. Considering intraspecific variation in responses is important to avoid misrepresenting potential effects of anthropogenic noise and to ensure the best management and mitigation of this pervasive pollutant.

White-handed gibbons discriminate context-specific song compositions

White-handed gibbons produce loud and acoustically complex songs when interacting with their neighbours or when encountering predators. In both contexts, songs are assembled from a small number of units although their composition differs in context-specific ways. Here, we investigated whether wild gibbons could infer the ‘meaning’ when hearing exemplars recorded in both contexts (i.e. ‘duet songs’ vs. ‘predator songs’). We carried out a playback experiment by which we simulated the presence of a neighbouring group producing either its duet or a predator song in order to compare subjects’ vocal and locomotor responses. When hearing a recording of a duet song, subjects reliably responded with their own duet song, which sometimes elicited further duet songs in adjacent groups. When hearing a recording of a predator song, however, subjects typically remained silent, apart from one of six groups which replied with its own predator song. Moreover, in two of six trials, playbacks of predator songs elicited predator song replies in non-adjacent groups. Finally, all groups showed strong anti-predator behaviour to predator songs but never to duet songs. We concluded that white-handed gibbons discriminated between the two song types and were able to infer meaning from them. We discuss the implications of these findings in light of the current debate on the evolutionary origins of syntax.