Disgust in animals and the application of disease avoidance to wildlife management and conservation.

Disgust is an adaptive system hypothesized to have evolved to reduce the risk of becoming sick. It is associated with behavioural, cognitive and physiological responses tuned to allow animals to avoid and/or get rid of parasites, pathogens and toxins. Little is known about the mechanisms and outcomes of disease avoidance in wild animals. Furthermore, given the escalation of negative human-wildlife interactions, the translation of such knowledge into the design of evolutionarily relevant conservation and wildlife management strategies is becoming urgent. Contemporary methods in animal ecology and related fields, using direct (sensory cues) or indirect (remote sensing technologies and machine learning) means, provide a flexible toolbox for testing and applying disgust at individual and collective levels. In this review/perspective paper, we provide an empirical framework for testing the adaptive function of disgust and its associated disease avoidance behaviours across species, from the least to the most social, in different habitats. We predict various trade-offs to be at play depending on the social system and ecology of the species. We propose five contexts in which disgust-related avoidance behaviours could be applied, including endangered species rehabilitation, invasive species, crop-raiding, urban pests and animal tourism. We highlight some of the perspectives and current challenges of testing disgust in the wild. In particular, we recommend future studies to consider together disease, predation and competition risks. We discuss the ethics associated with disgust experiments in the above contexts. Finally, we promote the creation of a database gathering disease avoidance evidence in animals and its applications.

Le dégoût est un système adaptatif supposé avoir évolué afin de réduire le risque de tomber malade. Il est associé à des réponses comportementales, cognitives et physiologiques adaptées pour permettre aux animaux d'éviter et/ou de se débarrasser des parasites, pathogènes et toxines. On sait peu de choses sur les mécanismes et les conséquences de l'évitement des maladies chez les animaux sauvages. Étant donné l'escalade des interactions négatives entre humains et faune, la traduction de ces connaissances dans la conception de stratégies de conservation et de gestion de la faune - prenant en considération l'évolution des espèces - devient urgente. Les méthodes contemporaines en écologie animale et dans les domaines connexes, utilisant des moyens directs (indices sensoriels) ou indirects (technologies de télédétection et apprentissage automatique), fournissent une boîte à outils flexible pour tester et appliquer le dégoût aux niveaux individuel et collectif. Dans cet article de revue/perspective, nous fournissons un cadre empirique pour tester la fonction adaptative du dégoût et les comportements associés d'évitement des maladies chez différentes espèces - des moins sociales aux plus sociales, et dans différents habitats. Nous prédisons divers compromis en fonction du système social et de l'écologie de l'espèce. Nous proposons cinq contextes dans lesquels les comportements d'évitement liés au dégoût pourraient être appliqués: la réhabilitation d'espèces menacées; les espèces envahissantes; les dommages aux cultures; les nuisibles urbains; et le tourisme animalier. Nous mettons en avant certaines perspectives et défis actuels de l'expérimentation sur le dégoût en milieu naturel. En particulier, nous recommandons la considération de plusieurs risques ensemble: maladie, prédation et compétition. Nous discutons également de l'éthique associée aux expériences sur le dégoût dans les contextes ci-dessus. Enfin, nous promouvons la création d'une base de données rassemblant les stratégies d'évitement des maladies chez les animaux et leurs applications.

Occupancy data improves parameter precision in spatial capture-recapture models.

Population size is one of the basic demographic parameters for species management and conservation. Among different estimation methods, spatially explicit capture-recapture (SCR) models allow the estimation of population density in a framework that has been greatly developed in recent years. The use of automated detection devices, such as camera traps, has impressively extended SCR studies for individually identifiable species. However, its application to unmarked/partially marked species remains challenging, and no specific method has been widely used. We fitted an SCR-integrated model (SCR-IM) to stone marten Martes foina data, a species for which only some individuals are individually recognizable by natural marks, and estimate population size based on integration of three submodels: (1) individual capture histories from live capture and transponder tagging; (2) detection/nondetection or "occupancy" data using camera traps in a bigger area to extend the geographic scope of capture-recapture data; and (3) telemetry data from a set of tagged individuals. We estimated a stone marten density of 0.352 (SD: 0.081) individuals/km2. We simulated four dilution scenarios of occupancy data to study the variation in the coefficient of variation in population size estimates. We also used simulations with similar characteristics as the stone marten case study, comparing the accuracy and precision obtained from SCR-IM and SCR, to understand how submodels' integration affects the posterior distributions of estimated parameters. Based on our simulations, we found that population size estimates using SCR-IM are more accurate and precise. In our stone marten case study, the SCR-IM density estimation increased the precision by 37% when compared to the standard SCR model as regards to the coefficient of variation. This model has high potential to be used for species in which individual recognition by natural markings is not possible, therefore limiting the need to rely on invasive sampling procedures.

The effectiveness of conditioned aversion in wolves: Insights from experimental tests.

It has been suggested that conditioned food aversion (CFA) could be a potential non-lethal intervention by which to deter attacks on livestock by large carnivores. CFA occurs when an animal associates the characteristics of a food with an illness, thus rejecting that food in subsequent encounters. CFA can be associated with an artificial odour during conditioning. Despite the debate surrounding the use of this intervention, more studies evaluating the effectiveness of CFA are necessary. We experimentally evaluated the potential of microgranulated levamisole + a vanilla odour cue to induce CFA in captive Iberian wolves (Canis lupus signatus). Four out of the five wolves treated showed an aversion to the meat for a minimum of one month after conditioning. The microgranulated presentation masked the flavour and smell of the levamisole but increased its volume, which may have facilitated its detection by the wolves. We also observed that the strength of the odour played an important role in the aversion extinction. The use of microgranulated levamisole + an odour cue has the potential to be used as an intervention by which to induce aversive conditioning in wolves in the wild, although rigorous field tests are required. We discuss the potential of CFA to deter attacks on livestock by large carnivores.

Conditioned food aversion in domestic dogs induced by thiram.

BACKGROUND: The conflict between predators and humans for resources such as game species or livestock is an ancient issue, and it is especially sharp in the case of medium-large wild canids. In order to manage this conflict, lethal control methods are often used, which can sometimes be illegal, such as poisoning. As an alternative, conditioned food aversion (CFA) is a non-lethal method to reduce predation in which animals learn to avoid a given food due to the adverse effects caused by the ingestion of an undetectable chemical compound added to this food. The present study aimed to test thiram as a CFA agent in penned dogs as a first approach to use this substance for reducing the predation conflict associated with wild canids. RESULTS: Thiram, with or without an additional odor cue, produced CFA in penned dogs for more than 2 months. Moreover, thiram seemed to be undetectable and safe after the third ingestion of a 40-60 mg kg-1 dose. Desirable adverse effects, such as vomits, appeared around 1 h after exposure. These characteristics make thiram optimal for its use in predation reduction through CFA. However, individual variability could prevent CFA acquisition by some animals. CONCLUSIONS: Thiram has the potential to be used as a CFA agent in wildlife management and conservation to reduce predation by wild canids. Since thiram produced CFA without the problems of detectability and toxicity caused by other substances, it may be an alternative to lethal control methods used to reduce predation on game, livestock and endangered species. © 2019 Society of Chemical Industry.

Selection of new chemicals to be used in conditioned aversion for non-lethal predation control.

Globally, native predators and scavengers are threatened through the incidence of illegal poisoning due to increasing human-wildlife conflicts. The use of conditioned taste aversion (CTA) may mitigate such conflicts. CTA is a robust learning paradigm that occurs when animals associate a food with a discomfort induced by a chemical, thereby avoiding that food in subsequent encounters. We reviewed the potential of 167 chemical compounds to be used in CTA, considering effects, margin of safety, accessibility, and detectability. After the review, 15 compounds fulfilled the required characteristics, but only five (thiabendazole, thiram, levamisole, fluconazole and fluralaner) were finally selected to be tested in CTA assays with dogs. Of the tested compounds, thiabendazole, thiram and levamisole caused target food rejection by dogs and reduced the time spent eating during post-conditioning. However, despite being microencapsulated, levamisole appeared to be detectable by dogs, whereas thiram and thiabendazole were not. Fluconazole and fluralaner did not produce any CTA effect. Thiabendazole, thiram and levamisole can therefore induce CTA, and thus are potential candidates as aversive compounds for wildlife management. Thiram is an undetectable, relatively safe and accessible compound that can induce CTA in canids, and opens new possibilities to develop methods of non-lethal predation control.

Generalized spatial mark-resight models with incomplete identification: An application to red fox density estimates.

The estimation of abundance of wildlife populations is an essential part of ecological research and monitoring. Spatially explicit capture-recapture (SCR) models are widely used for abundance and density estimation, frequently through individual identification of target species using camera-trap sampling.Generalized spatial mark-resight (Gen-SMR) is a recently developed SCR extension that allows for abundance estimation when only a subset of the population is recognizable by artificial or natural marks. However, in many cases, it is not possible to read the marks in camera-trap pictures, even though individuals can be recognized as marked. We present a new extension of Gen-SMR that allows for this type of incomplete identification.We used simulation to assess how the number of marked individuals and the individual identification rate influenced bias and precision. We demonstrate the model's performance in estimating red fox (Vulpes vulpes) density with two empirical datasets characterized by contrasting densities and rates of identification of marked individuals. According to the simulations, accuracy increases with the number of marked individuals (m), but is less sensitive to changes in individual identification rate (δ). In our case studies of red fox density estimation, we obtained a posterior mean of 1.60 (standard deviation SD: 0.32) and 0.28 (SD: 0.06) individuals/km2, in high and low density, with an identification rate of 0.21 and 0.91, respectively.This extension of Gen-SMR is broadly applicable as it addresses the common problem of incomplete identification of marked individuals during resighting surveys.