Smart carnivores think twice: Red fox delays scavenging on conspecific carcasses to reduce parasite risk

Abstract

The recent SARS-CoV-2 epidemic has highlighted the need to prevent emerging and re-emerging diseases, which means that we must approach the study of diseases from a One Health perspective. The study of pathogen transmission in wildlife is challenging, but it is unquestionably key to understand how epidemiological interactions occur at the wildlife-domestic-human interface. In this context, studying parasite avoidance behaviours may provide essential insights on parasite transmission, host-parasite coevolution, and energy flow through food-webs. However, the strategies of avoiding trophically transmitted parasites in mammalian carnivores have received little scientific attention. Here, we explore the behaviour of red foxes (Vulpes vulpes) and other mammalian carnivores at conspecific and heterospecific carnivore carcasses using videos recorded by camera traps. We aim to determine 1) the factors influencing the probability of foxes to practice cannibalism, and 2) whether the scavenging behaviour of foxes differ when facing conspecific vs. heterospecific carcasses. We found that red foxes were generally reluctant to consume mesocarnivore carrion, especially of conspecifics. When recorded, consumption by foxes was delayed several days (heterospecific carcasses) or weeks (conspecific carcasses) after carcass detection. Other mammalian scavengers showed a similar pattern. Also, meat-borne parasite transmission from wild carnivore carcasses to domestic dogs and cats was highly unlikely. Our findings challenge the widespread assumption that cannibalistic or intra-specific scavenging is a major transmission route for Trichinella spp. and other meat-borne parasites, especially for the red fox. Overall, our results suggest that the feeding decisions of scavengers are probably shaped by two main contrasting forces, namely the nutritional reward provided by carrion of phylogenetically similar species and the risk of acquiring meat-borne parasites shared with these species. This study illustrates how the detailed monitoring of carnivore behaviour is essential to assess the epidemiological role of these hosts in the maintenance and dispersion of parasites of public and animal health relevance.

Keywords: Cannibalism; Carnivore; Carrion; Landscape of disgust; Parasite avoidance behaviour; Parasite transmission risk.

Graphical abstract

Fig. 1

Weekly variation in consumption patterns of mesocarnivore carcasses by red fox and other mammalian scavengers in three areas of southeastern Spain. A) Weekly percentage of consumed (“cons.”; i.e., with at least one consumption event) and non-consumed (“non-cons.”; i.e., visited, but no consumption events recorded) carcasses by red fox and other mammalian scavengers per study area and carcass type. B) Weekly number of consumption (“cons.”) and non-consumption (“non-cons.”) events by red fox and other mammalian scavengers per study area and carcass type. For a given week, the number of events are divided by the grand total number of carcasses studied in each study area. The number of carcasses available each week to scavengers is given in parentheses. Panels for carcasses of carnivores other than foxes are in boxes.

Fig. 2

Weekly variation in the ratios consumed:non-consumed carcasses and consumption:non-consumption events by the red fox per study area and carcass type. Values above and below the dashed horizontal grey line indicate, respectively, ratios biased towards consumption and non-consumption. For a given week, the number of carcasses available to scavengers is given in parentheses. Panel for carcasses of carnivores other than foxes is in the box.

Fig. 3

Conceptual model showing how food quality and safety shape the propensity of mammalian carnivores to scavenge on carcasses of species differing in their phylogenetic distance to the consumer. A) On one hand, the nutritive value, which is maximum for conspecific carcasses, decreases with time. Note that all meat can be regarded as high- to very high-quality food for a carnivore (Swift et al., 1979). B) On the other hand, the probability of a carcass to have fewer infective stages of meat-borne parasites increases with time. In fresh carcasses, the risk for a consumer of acquiring meat-borne parasites, at least for direct life cycle parasites, is maximum when it ingests conspecific carrion, and minimum for carcasses belonging to weakly related species, with which the number of shared parasite species is lowest. Non-linearity is probably a fundamental property of all of these functions. C) These contrasting forces probably shape the observed patterns of carcass consumption (for our study areas, see this study, Arrondo et al., 2019, Moleón et al., 2017, Morales-Reyes et al., 2017, Muñoz-Lozano et al., 2019).