The ecology of zoonotic parasites in the Carnivora

Despite nearly half of the Carnivora being zoonotic hosts, and their ubiquity across all major biomes globally, there remain surprising gaps in basic biological ecological knowledge this group that preclude deeper assessments diversity risk.Functional traits related to dietary suggest hosts reflect an omnivorous life history strategy with potentially profound implications for infection tolerance.The will experience widespread changes global range distributions unpredictable significant impacts on biotic interactions, cascading effects disease risk from carnivore as well prey species.Filling research functional ecology improve our understanding roles sentinels, regulators, sinks, or sources parasites. The order includes over 300 species vary many orders magnitude size inhabit biomes, tropical rainforests polar seas. high parasites represents a source potential emerging diseases humans. Zoonotic may be driven part by exceptionally host behavioral, physiological, traits. We review macroecological patterns within carnivores, explore serve synthesize theoretical empirical future work carnivores multipliers, sentinels timely frontiers. In ecology, 'functional diversity' refers ways organisms contribute overall functioning communities ecosystems [1.Petchey O.L. Gaston K.J. Functional diversity: back basics looking forward.Ecol. Lett. 2006; 9: 741-758Crossref PubMed Scopus (1478) Google Scholar]. With 302 extant speciesi, is not most species-rich among mammals (that distinction belongs Rodentia, rodents, Chiroptera, bats), but it functionally diverse [2.Macdonald D.W. velvet claw: natural carnivores. BBC, 1993Google This manifested exceptional Scholar,3.Kim S. et al.Comparison carnivore, omnivore, herbivore mammalian genomes new leopard assembly.Genome Biol. 2016; 17: 211Crossref (56) Scholar], which influences aspects biology, history, including suitability pathogens. Curiously, collectively carry larger number known pathogens than any other mammal (hereafter, parasites; see Glossary) [4.Han B.A. al.Global mammals.Trends Parasitol. 32: 565-577Abstract Full Text PDF (190) despite having fewer rodents (2590 species) bats (1430 species). posit outcome observed Carnivora, adaptations support have exposed parasite disproportionate diversity. Here we recent literature reanalyze relevant published data occurrence identify better current risks order. Carnivorans (members hereafter carnivores) 182 causing 46 unique zoonoses Scholar] (see Table S1 supplemental information online). majority these are four types (56 bacteria, 25 viruses, 66 helminths, 28 protozoa; 1).Table 1The found 15 familiesFamilyaThere 56 protozoa families (photos example each family). exclude Prionodontidae, family zoonoses. Less common (e.g., prions) represented. Data image attributions reported S2. detailed here can S1.Common names countsZoonotic parasitesAiluridaeRed pandasSpecies: 2 Hosts: 18Bacteria: 0Helminths: 4Protozoa: 4Viruses: 0CanidaeDogs, foxesSpecies: 39Hosts: 1591Bacteria: 28Helminths: 37Protozoa: 15Viruses: 10EupleridaeFossasSpecies: 7Hosts: 11Bacteria: 0Protozoa: 1Viruses: 0FelidaeCatsSpecies: 46Hosts: 1647Bacteria: 15Helminths: 18Protozoa: 8Viruses: 4HerpestidaeMongooses, meerkatsSpecies: 35Hosts: 712Bacteria: 5Helminths: 2Protozoa: 2Viruses: 3HyaenidaeHyenasSpecies: 4Hosts: 27Bacteria: 5Protozoa: 1MephitidaeSkunksSpecies: 11Hosts: 312Bacteria: 1Protozoa: 4MustelidaeWeasels, badgers, ottersSpecies: 64Hosts: 2152Bacteria: 16Protozoa: 11Viruses: 5NandiniidaeAfrican palm civetSpecies: 1Hosts: 0OdobenidaeWalrusesSpecies: 13Bacteria: 1Helminths: 0Viruses: 0OtariidaeEared sealsSpecies: 15Hosts: 715Bacteria: 6Helminths: 0PhocidaeEarless 18Hosts: 819Bacteria: 4Helminths: 3Protozoa: 3Viruses: 7ProcyonidaeRaccoons, coatis, kinkajousSpecies: 13Hosts: 640Bacteria: 19Helminths: 5Viruses: 10UrsidaeBearsSpecies: 8Hosts: 532Bacteria: 13Helminths: 6Protozoa: 6ViverridaeGenets, civets, binturongsSpecies: 36Hosts: 717Bacteria: 6Viruses: 3a There S1. Open table tab also categorized into transmission modes (defined per [5.Stephens P.R. Mammal Parasite Database version 2.0.Ecology. 2017; 98: 1476Crossref (59) Scholar]):1.Close-contact requires proximity, occurs through behaviors such grooming, scratching, biting (rabies, SARS-CoV-2).2.Non-close-contact contact infectious particles persist environment, contaminated food water (Leptospira, [6.Millán J. al.Carriage pathogenic Leptospira at wild/domestic interface.Pol. Vet. Sci. 2019; 22: 589-598PubMed Scholar]).3.Zoonotic vector-borne transmitted arthropods, ticks (Borrelia burgdorferi, Lyme disease, [7.López-Pérez A.M. al.Molecular evidence Borrelia burgdorferi sensu stricto Rickettsia massiliae collected domestic–wild interface Chihuahua, Mexico.Ticks Tick Borne Dis. 10: 1118-1123Crossref (18) Scholar,8.Gherman C.M. al.First report lato two threatened carnivores: marbled polecat, Vormela peregusna European mink, Mustela lutreola (Mammalia: Mustelidae).BMC Res. 2012; 8: 137Crossref (21) Scholar]), mosquitoes (Francisella tularensis, tularemia, [9.Abdellahoum Z. al.Tularemia mosquito-borne disease.Microorganisms. 2020; 26Crossref (5) fleas (Yersinia pestis, plague, [10.Matchett M.R. al.Enzootic plague reduces black-footed ferret (Mustela nigripes) survival Montana.Vector 2010; 27-35Crossref (86) Scholar]).4.The numerous complex cycles require both intermediate definitive often use trophic transmission, where consumption stages. refer mode 'intermediate transmission' maintain previous naming conventions (as Scholar]). used directly determine play maintaining transmitting For instance, bridge (SARS-CoV-2, Box 1) reservoir Scholar,11.Viana M. al.Assembling identifying reservoirs infection.Trends Ecol. Evol. 2014; 29: 270-279Abstract (147) Scholar,12.Prager K.C. al.Rabies virus canine distemper wild domestic Northern Kenya: dogs reservoir?.Ecohealth. 483-498Crossref (37) While transmit humans, only involved populations wild. example, northern Kenya, serological rabies important repeatedly seed spillover African dogs, black-backed jackals, spotted striped hyenas, lions [12.Prager sub-Saharan Africa, domesticated guinea worm (Dracunculus medinensis) [13.Richards R.L. al.Identifying correlates Guinea dog populations.PLoS Negl. Trop. 14e0008620Crossref (6) helminth has cycle copepods (aquatic crustaceans) infected larvae. These larvae develop adult worms when they trophically suitable nonhuman primates, cats [14.McDonald R.A. al.Ecology Canis familiaris Dracunculus medinensis infection.PLoS 14e0008170Crossref (25) do become consuming water, scavenging remains fish frogs (prepared humans), system complicating ongoing efforts eradication Scholar].Box 1Potential SARS-CoV-2 carnivoresFollowing initial likely bat human, spilled humans animals. Nearly confirmed spillback [85.Gryseels al.Risk human-to-wildlife SARS-CoV-2.Mammal Rev. 8e00373-17Google some capacity onward (zoonotic capacity). farmed mink 11 countries North America Europeii, leading mortality lethal culling 17 million Denmark [86.Boklund A. al.SARS-CoV-2 Danish farms: course epidemic descriptive analysis outbreaks 2020.Animals. 2021; 1133445704Crossref (39) Scholar,87.Larsen H.D. al.Preliminary outbreak farmers associated community spread, Denmark, June November 2020.Euro Surveill. 26: 2100009Crossref (52) second time [88.Oude Munnink B.B. al.Transmission farms between humans.Science. 371: 172-177Crossref (376) been USA (presumed escaped mink)iii,iv [89.Shriner Exposure Utah, USA.Emerg. Infect. 27: 988-990Crossref (28) Scholar].A predicted 5400 integrating structural models three-dimensional virus–host protein–protein interactions machine-learning species’ [52.Fischhoff I.R. al.Predicting SARS-CoV-2.bioRxiv. (Posted online February 19, 2021)https://doi.org/10.1101/2021.02.18.431844PubMed identified several large geographic ranges: red fox (Vulpes, ~50 countries), polecat putorius), raccoon (Nyctereutes procyonoides), stoat erminea), wolf (Canis lupus). Notably, SARS-CoV-2, laboratory mice [90.Montagutelli X. al.The B1.351 P.1 variants extend mice.bioRxiv. March 18, 2021. 2021.03.18.436013)Google deer (P. maniculatus), experimentally [91.Fagre infection, neuropathogenesis mice: Implications New World rodents.PLoS Pathog. 17e1009585Crossref (24) Scholar,92.Griffin B.D. American mouse.Nat. Commun. 12: 3612Crossref (19) Scholar].Carnivores highest likelihood exposure occur close proximity human COVID-19 cases (Figure I). inset map (adapted Scholar]) shows particularly richness Southeast Asia Eastern Europe, people because (red fox, V. vulpes; Asiatic black bears, Ursus thibetanus; N. procyonoides) live traded (grey wolf, lupus; jaguar, Panthera onca) [93.Can Ö.E. al.Dealing deadly pathogens: Taking stock legal trade wildlife health.Glob. Conserv. 17e00515PubMed Scholar]i.Ongoing increases sylvatic perpetuate secondary spillovers novel Scholar,91.Fagre Scholar,94.Franklin A.B. Bevins S.N. Spillover America: A conceptual model perpetuation pathogen.Sci. Total Environ. 733: 139358Crossref (43) Spillback further threaten declining endangered speciesv, grizzly bear (Ursus arctos, listed threatened), maritimus, vulnerable), lupus, endangered), giant panda (Ailuropoda melanoleuca, vulnerable) (Ailurus fulgens, susceptible regularly handled biologists managers. Following Carnivores Scholar]i. Ongoing encounter modes, one intuitive prediction exemplified predominate given carnivory distinguishing feature idea gives rise ancillary hypotheses. One hypothesis predators bioaccumulate [15.Malmberg J.L. al.Bioaccumulation pathogen top predators.Trends 36: 411-420Abstract (4) positive relationship items richness. scale degree carnivory, measured either percentage diet composed meat. An absence pattern (no carnivory) could possess protecting them higher encountered via [16.Nunn C.L. al.A comparative study white blood cell counts carnivores.Proc. R. Soc. Lond. Ser. B 2003; 270: 347-356Crossref (71) Scholar,17.Moleón al.Carnivore carcasses avoided carnivores.J. Anim. 86: 1179-1191Crossref (33) Similarly, confirmation carnivory–parasite without corresponding would tolerance hosts. include, immune strategies behavioral minimize sequestration gut flora enable harbor physiological damage [18.Schneider D.S. Ayres J.S. Two survive infection: what resistance teach us about treating diseases.Nat. Immunol. 2008; 889-895Crossref (0) Transmission strongly underlie risk, infect cause [19.Plowright R.K. al.Pathways spillover.Nat. Microbiol. 15: 502-510Crossref (331) human-centric perspective, shared [20.Vogel G. Conservation biology. Can great apes saved Ebola?.Science. 300: 1645Crossref (14) Scholar, 21.Bicca-Marques J.C. de Freitas role monkeys, mosquitoes, yellow fever fragmented landscape South Brazil: howler monkeys matter public health.Trop. 3: 78-89Crossref 22.Hoffmann C. al.Persistent anthrax driver rainforest.Nature. 548: 82-86Crossref (55) topic wake pandemic human-adapted coronavirus caused least species, (Box 1). Thus, anthroponosis, animals predominantly pathogen, pose particular overlap human-dominated landscapes, zoos. Previous approximately 46% (140/302 currently out 16 families, Mustelidae (weasels, otters relatives) Felidae (cats) harboring Canidae (dogs) greatest (the rare understudied family, harbors none) (Table general, terrestrial foraging more marine effort devoted average Web Science search hits; available S3). groups expected cluster phylogenetically since successful depends rates [23.McCallum H. al.Breaking beta: deconstructing function.Philos. Trans. 372: 20160084Crossref (58) 24.Han al.Infectious behavioural allometry mammals.J. 2015; 84: 637-646Crossref (32) 25.LoScerbo D. al.Phylogenetically conserved local abiotic conditions jointly drive geography intensity.Funct. 34: 2477-2487Crossref (2) 26.Fountain-Jones N.M. al.Trophic position determines phylogenetic recovery after disturbance community.Funct. 31: 1441-1451Crossref (15) widely strict endotherm cheetah, Felidae) herbivores panda, Ursidae), influence acquired (prey vs. plants). Sociality living affect dynamics spread wolves, [24.Han Scholar,27.Brandell E.E. metapopulation social applied Yellowstone wolves.Proc. Natl. Acad. U. e2020023118Crossref (3) contrast, ursids (bears) mustelids