Bioaccumulation of Pathogen Exposure in Top Predators

Malmberg, Jennifer L.; White, Lauren A.; VandeWoude, Sue

doi:10.1016/j.tree.2021.01.008

Cited by 17 publications

(15 citation statements)

References 85 publications

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“…The mammalian order Carnivora is characterized by a large diversity of members, which include both terrestrial and aquatic species that naturally occur in all continents and oceans [ 36 ]. Because of their feeding behavior, which involves hunting and carcass scavenging, these animals are constantly exposed to a high number of infectious agents and play a crucial role in disease spread, especially considering that many carnivore parasites are multi-host, i.e., capable of infecting multiple species [ 37 , 38 ]. Identifying microorganisms of carnivores and studying their host distribution and transmission dynamics has, therefore, important implications for animal health and conservation programs [ 39 ], especially since cross-species transmission does happen frequently and sometimes with catastrophic consequences [ 37 , 40 ].…”

Section: Discussionmentioning

confidence: 99%

“…Because of their feeding behavior, which involves hunting and carcass scavenging, these animals are constantly exposed to a high number of infectious agents and play a crucial role in disease spread, especially considering that many carnivore parasites are multi-host, i.e., capable of infecting multiple species [ 37 , 38 ]. Identifying microorganisms of carnivores and studying their host distribution and transmission dynamics has, therefore, important implications for animal health and conservation programs [ 39 ], especially since cross-species transmission does happen frequently and sometimes with catastrophic consequences [ 37 , 40 ]. In this manuscript, we fully characterized and investigated the epidemiology and host distribution of Newlavirus, a novel parvovirus we discovered in foxes.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Newlavirus, a Novel, Highly Prevalent, and Highly Diverse Protoparvovirus of Foxes (Vulpes spp.)

Canuti

Bouchard

Rodrigues

et al. 2021

Viruses

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The genus Protoparvovirus (family Parvoviridae) includes several viruses of carnivores. We describe a novel fox protoparvovirus, which we named Newlavirus as it was discovered in samples from Newfoundland and Labrador, Canada. Analysis of the full non-structural protein (NS1) sequence indicates that this virus is a previously uncharacterized species. Newlavirus showed high prevalence in foxes from both the mainland (Labrador, 54/137, 39.4%) and the island of Newfoundland (22/50, 44%) but was not detected in samples from other carnivores, including coyotes (n = 92), lynx (n = 58), martens (n = 146), mink (n = 47), ermines (n = 17), dogs (n = 48), and ringed (n = 4), harp (n = 6), bearded (n = 6), and harbor (n = 2) seals. Newlavirus was found at similar rates in stool and spleen (24/80, 30% vs. 59/152, 38.8%, p = 0.2) but at lower rates in lymph nodes (2/37, 5.4%, p < 0.01). Sequencing a fragment of approximately 750 nt of the capsid protein gene from 53 samples showed a high frequency of co-infection by more than one strain (33.9%), high genetic diversity with 13 genotypes with low sequence identities (70.5–87.8%), and no geographic segregation of strains. Given the high prevalence, high diversity, and the lack of identification in other species, foxes are likely the natural reservoir of Newlavirus, and further studies should investigate its distribution.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Newlavirus, a Novel, Highly Prevalent, and Highly Diverse Protoparvovirus of Foxes (Vulpes spp.)

Canuti

Bouchard

Rodrigues

et al. 2021

Viruses

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“…This idea gives rise to ancillary hypotheses. One hypothesis is that predators in this group bioaccumulate the parasites of their prey [15], leading to a positive relationship between the diversity of prey items and parasite richness. A related hypothesis is that the number of zoonotic parasites observed in carnivores will scale with the degree of carnivory, measured as either prey diversity or the percentage of diet composed of meat.…”

Section: Glossarymentioning

confidence: 99%

The ecology of zoonotic parasites in the Carnivora

Han

Castellanos

Schmidt

et al. 2021

Trends in Parasitology

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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).

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“…Most empirical and theoretical research has focused on the ecological role of predators in regulating prey pathogens by targeting infected prey (which are easier to catch), or altering prey community structures. Nevertheless, there are numerous well-documented examples of spillover from prey to predators, with some carnivore populations suffering catastrophic declines (Malmberg et al, 2021). Predator exposure to prey pathogens can be conceptualized as a form of bioaccumulation (Malmberg et al, 2021).…”

Section: Spillover From Prey To Predatorsmentioning

confidence: 99%

Homo medicus: The transition to meat eating, increased pathogen pressure, and the constitutive and inducible use of pharmacological plants in Homo

Hagen¹,

Blackwell²,

Lightner³

et al. 2021

Preprint

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The human lineage entered a more carnivorous niche 2.6 mya. A range of evidence indicates this increased zoonotic pathogen pressure. This evidence includes increased zoonotic infections modern hunter-gatherers and bushmeat hunters relative to others living in the same environments, exceptionally low stomach pH compared to other primates, human-specific downregulation in ANTXR2 that would have protected against increased exposure to zoonotic anthrax, exceptional human immune responses to LPS compared to other primates, and other divergent immune genes. These all point to change, and likely intensification, in the disease environment of Homo compared to earlier hominins and other apes. At the same time, the brain, an organ in which inflammatory immune responses are highly constrained, begins to increase, eventually tripling in size. We propose that the combination of increased zoonotic pathogen pressure and the challenges of defending a large brain and body from pathogens across what would eventually become the longest lifespan of any mammal, selected for intensification of the self-medication strategies already in place in apes and other primates, resulting in a variety of plant-based pathogen defenses. In support, there is evidence of medicinal plant use by hominins in the middle Paleolithic, and all cultures today have sophisticated, plant-based medical systems, incorporate plant components high in secondary compounds (spices) into food, and regularly consume psychoactive substances that are harmful to helminths and other pathogens in the CNS and other tissues. The computational challenges of discovering effective plant-based treatments, and the economic challenges of benefiting from costly-to- acquire medical knowledge that would be more often useful to others than oneself, were selection pressures for increased cognitive abilities and unique exchange relationships in Homo. In the story of human evolution, which has long featured hunters, shamans and healers had an equal role to play.

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Bioaccumulation of Pathogen Exposure in Top Predators

Abstract: Advances in pathogen detection technologies have allowed more thorough characterization of infections in freeranging wildlife.

Cited by 17 publications

References 85 publications

Newlavirus, a Novel, Highly Prevalent, and Highly Diverse Protoparvovirus of Foxes (Vulpes spp.)

Newlavirus, a Novel, Highly Prevalent, and Highly Diverse Protoparvovirus of Foxes (Vulpes spp.)

The ecology of zoonotic parasites in the Carnivora

Homo medicus: The transition to meat eating, increased pathogen pressure, and the constitutive and inducible use of pharmacological plants in Homo

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