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.

Carcass appearance does not influence scavenger avoidance of carnivore carrion

“…Bobcats ( Lynx rufus ) entirely avoided scavenging on intact coyote carrion (paired and unpaired), whereas they consumed a large proportion of the intact wild pig carcasses they scavenged (Table S1 ), and coyotes generally avoided scavenging on conspecifics for intact carcasses. Together, these findings support our first hypothesis and the findings of other studies that carnivore carrion is typically avoided by conspecific and intraguild species 12 , 16 , 17 , 28 . More similar species (i.e., phylogenetically and ecologically) harbor comparable parasite assemblages 38 and therefore it is assumed that mammalian carnivores likely avoid cannibalizing and scavenging on other carnivores due to perceived disease risks 28 .…”

“…Several scavenging studies have used carcasses that were not fully intact including partially or fully skinned, eviscerated, and/or head and feet removed 18 , 27 , 28 . Yet, few of these assessed how these alterations, and thus external characteristics and associated chemical stimuli, influence scavengers’ feeding decisions (but see Moleón et al 12 and Selva et al 29 ), and most had limited sample sizes.…”

Epidemiology of Trichinella infection in wild boar from Spain and its impact on human health during the period 2006–2019

“…Nevertheless, the growing number of wild boar is apparently not paralleled by a higher prevalence of Trichinella infection in this particular host; however, caution is needed, since wild boar sampling was locally suboptimal. Ultimately, the prevalence of Trichinella infection in wild boar may reflect two important factors in the epidemiology of this group of parasites: the presence of Trichinella britovi , a carnivore-adapted species, whose larvae survive only a few weeks/months in the muscles of swine ( Pozio et al, 2020 ), and the reduction of the scavenger activity of reservoir animals ( Gonzálvez et al, 2021 ), i.e. the main form of Trichinella transmission, when abundant anthropogenic food resources are available.…”

Integrating terrestrial scavenging ecology into contemporary wildlife conservation and management

“…Striped skunks ( Mephitis mephitis ) were the primary scavenger consuming bats, but raccoons, gray foxes ( Urocyon cinereoargenteus ), and domestic cats also consumed bat carcasses, acting as potential vectors for the rabies virus. Although recent studies have elucidated the complexities associated with the landscapes of fear and disgust and scavenging of conspecifics, there are still areas to investigate such as animal responses to signals associated with parasite risk (Gonzálvez et al, 2021 ), and parasite risk in relation to carcass size, ecosystem type, and season (Moleón & Sánchez‐Zapata, 2021 ). In addition to vertebrate scavengers, we advocate for further studies on invertebrates that visit carrion, such as carrion flies (Hall et al, 2019 ), ants, and mosquitoes, for a holistic contribution to understanding disease spread in relation to scavenging.…”