Understanding potential implications for non-trophic parasite transmission based on vertebrate behavior at mesocarnivore carcass sites

High infection risk is often associated with aggregations of animals around attractive resources. Here, we explore the behavior of potential hosts of non-trophically transmitted parasites at mesocarnivore carcass sites. We used videos recorded by camera traps at 56 red fox (Vulpes vulpes) carcasses and 10 carcasses of other wild carnivore species in three areas of southeastern Spain. Scavenging species, especially wild canids, mustelids and viverrids, showed more frequent rubbing behavior at carcass sites than non-scavenging and domestic species, suggesting that they could be exposed to a higher potential infection risk. The red fox was the species that most frequently contacted carcasses and marked and rubbed carcass sites. Foxes contacted heterospecific carcasses more frequently and earlier than conspecific ones and, when close contact occurred, it was more likely to be observed at heterospecific carcasses. This suggests that foxes avoid contact with the type of carcass and time period that have the greatest risk as a source of parasites. Overall, non-trophic behaviors of higher infection risk were mainly associated with visitor-carcass contact and visitor contact with feces and urine, rather than direct contact between visitors. Moreover, contact events between scavengers and carnivore carcasses were far more frequent than consumption events, which suggests that scavenger behavior is more constrained by the risk of acquiring meat-borne parasites than non-trophically transmitted parasites. This study contributes to filling key gaps in understanding the role of carrion in the landscape of disgust, which may be especially relevant in the current global context of emerging and re-emerging pathogens. Graphical abstract

Exploring Vertebrate Behavior at Mesocarnivore Carcass Sites: Implications for Non-Trophic Parasite Transmission

The spatiotemporal distribution of parasites in ecosystems is heterogeneous. High infection risk is often associated with aggregations of animals around attractive resources. Here, we explore the behavior of potential hosts of non-trophically transmitted parasites at mesocarnivore carcass sites. We used videos recorded by camera traps at 56 red fox (Vulpes vulpes) carcasses and 10 carcasses of other wild carnivore species in three areas of southeastern Spain. In general, scavenging species, especially wild canids, mustelids and viverrids that display rubbing behavior, were more exposed to infection risk at carnivore carcass sites than non-scavenging and domestic species. The red fox was the species that most frequently contacted carcasses and marked and rubbed carcass sites. Foxes contacted heterospecific carcasses more frequently and earlier than conspecific ones, and close contact was more frequently observed at heterospecific carcasses. Thus, foxes seemed to avoid contacting carcasses in those periods and at carcass types of maximum risk of acquiring parasites. Overall, our results suggest that infection risk at carnivore carcass sites may take place mainly for visitor-carcass contact or contact with feces and urine rather than direct contact between visitors. Moreover, contact events between scavengers and carnivore carcasses are far more frequent than consumption events, which indicates that scavenger behavior is more constrained by the risk of acquiring meat-borne parasites than non-trophically transmitted parasites. This study contributes to filling key gaps in understanding the role of carrion in the landscape of disgust, which may be especially relevant in the current global context of emerging and re-emerging pathogens.

Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Identifying a key host in an acanthocephalan-amphipod system

SUMMARYTrophically transmitted parasites may use multiple intermediate hosts, some of which may be ‘key-hosts’, i.e. contributing significantly more to the completion of the parasite life cycle, while others may be ‘sink hosts’ with a poor contribution to parasite transmission. Gammarus fossarum and Gammarus roeseli are sympatric crustaceans used as intermediate hosts by the acanthocephalan Pomphorhynchus laevis. Gammarus roeseli suffers higher field prevalence and is less sensitive to parasite behavioural manipulation and to predation by definitive hosts. However, no data are available on between-host differences in susceptibility to P. laevis infection, making it difficult to untangle the relative contributions of these hosts to parasite transmission. Based on results from estimates of prevalence in gammarids exposed or protected from predation and laboratory infections, G. fossarum specimens were found to be more susceptible to P. laevis infection. As it is more susceptible to both parasite infection and manipulation, G. fossarum is therefore a key host for P. laevis transmission.

Effect of habitat use and diet on the gastrointestinal parasite community of an avian omnivore from an urbanized environment

With urbanization, anthropogenic foods have grown in importance for several species. A shift away from natural foods is likely to affect trophically transmitted parasites, although this has received limited attention in urban-adapted avian omnivores. We examined the effect of habitat use and diet on gastrointestinal parasite assemblages of Ring-billed Gulls (Larus delawarensis Ord, 1815) breeding in an urbanized region (Montréal, Quebec, Canada) using three approaches depicting different temporal scales. Birds were fitted with global positioning system data loggers to determine habitat-use patterns during a 2–3 day period. Stomach contents were examined, providing dietary information during the preceding hours. Liver carbon (δ13C) and nitrogen (δ15N) stable isotope signatures served as proxy of nutrient assimilation during the preceding 10 days. Endoparasite community variations were best explained by δ13C and δ15N ratios. Individuals with lower δ15N had lower parasite abundance, while δ13C was enriched in birds with less diverse parasites (fewer helminth genera). Tissue depletion in15N in Ring-billed Gulls from this colony has previously been associated with predominant consumption of human-related foods. The present study supports the hypothesis that Ring-billed Gulls exhibiting preference for anthropogenic food sources encounter fewer trophically transmitted parasites, which may have contributed, in part, to their population expansion during the last century.