The ecology of zoonotic parasites in the Carnivora

Abstract

The order Carnivora includes over 300 species that vary many orders of magnitude in size and inhabit all major biomes, from tropical rainforests to polar seas. The high diversity of carnivore parasites represents a source of potential emerging diseases of humans. Zoonotic risk from this group may be driven in part by exceptionally high functional diversity of host species in behavioral, physiological, and ecological traits. We review global macroecological patterns of zoonotic parasites within carnivores, and explore the traits of species that serve as hosts of zoonotic parasites. We synthesize theoretical and empirical research and suggest future work on the roles of carnivores as biotic multipliers, regulators, and sentinels of zoonotic disease as timely research frontiers. Zoonotic and functional diversity in the CarnivoraIn ecology, 'functional diversity' refers to the many ways that organisms contribute to the overall functioning of communities and ecosystems [1]. With 302 extant species i , the order Carnivora is not the most species-rich among mammals (that distinction belongs to the orders Rodentia, the rodents, and Chiroptera, the bats), but it is among the most functionally diverse [2]. This functional diversity is manifested in exceptional dietary diversity [2,3], which influences all aspects of carnivore biology, ecology, and life history, including their suitability as hosts of parasites and pathogens.Curiously, carnivores collectively carry a larger number of known zoonotic pathogens and parasites than any other mammal group (hereafter, zoonotic parasites; see Glossary) [4], despite having an order of magnitude fewer species than rodents (2590 extant species) or bats (1430 extant species). We posit that this zoonotic diversity is the outcome of high functional diversity observed in the Carnivora, in which ecological adaptations to support high dietary diversity have exposed this order to a parasite diversity that is disproportionate to their species diversity. Here we review recent literature and reanalyze relevant published data to explore the occurrence of zoonotic parasites and their hosts within the order Carnivora, and to identify research gaps that preclude a better understanding of current and future zoonotic risks in this order. Transmission of zoonotic parasites in the CarnivoraCarnivorans (members of the order Carnivora, hereafter carnivores) host 182 known zoonotic parasite species causing 46 unique zoonoses [4] (see Table S1 in the supplemental information online). The majority of these parasites are of four major types (56 bacteria, 25 viruses, 66 helminths, and 28 protozoa; Table 1).Zoonotic parasites can also be categorized into four transmission modes (defined as per [5]):1. Close-contact transmission requires proximity, and transmission occurs through behaviors such as grooming, scratching, or biting (rabies, SARS-CoV-2).

Carcass appearance does not influence scavenger avoidance of carnivore carrion

“…Therefore, carnivores may avoid scavenging within their guild due to potential health risks from more specialized illnesses like canine distemper and parvovirus. Further, carnivores might bioaccumulate more diseases due to their diverse diets 44,45 . In addition, species in the order Carnivora (307 extant species 46 ) collectively carry more zoonotic diseases than the largest order of mammals, rodents (2,623 extant species 46 ) 47 .…”

Zoonotic parasites associated with predation by dogs and cats

“…Recent extrinsic factors (e.g. environmental and climate modifications, urbanization, habitat fragmentation) have favored the trophic transmission of parasites [ 88 , 89 ]. This has resulted in an increased risk of spill-over of parasites from wild to peri-urban and urban settings favoring the contact of predators and prey, along with the parasites they carry.…”

The one health perspective to improve environmental surveillance of zoonotic viruses: lessons from COVID-19 and outlook beyond

“…Foraging behaviours are a key source of cross-species transmission of disease between animal species (as well as humans). Carnivores are hypothesised to accumulate pathogens through their prey, and hence have a parasite richness that correlates to the diversity of prey in their respective diets [ 66 ]. Consequences of frequent exposure to pathogens include immunological adaptations such as greater white blood cell count in top predators [ 67 ].…”