Population fluctuations and synanthropy explain transmission risk in rodent-borne zoonoses (original) (raw)

Abstract

Population fluctuations are widespread across the animal kingdom, especially in the order Rodentia, which includes many globally important reservoir species for zoonotic pathogens. The implications of these fluctuations for zoonotic spillover remain poorly understood. Here, we report a global empirical analysis of data describing the linkages between habitat use, population fluctuations and zoonotic reservoir status in rodents. Our quantitative synthesis is based on data collated from papers and databases. We show that the magnitude of population fluctuations combined with species' synanthropy and degree of human exploitation together distinguish most rodent reservoirs at a global scale, a result that was consistent across all pathogen types and pathogen transmission modes. Our spatial analyses identified hotspots of high transmission risk, including regions where reservoir species dominate the rodent community. Beyond rodents, these generalities inform our understanding of how natural and anthropogenic factors interact to increase the risk of zoonotic spillover in a rapidly changing world. Rodents are globally abundant and famous for extreme population fluctuations that manifest as boom-and-bust events, eruptive outbreaks and/or cycles . The contributors to these fluctuations are heterogeneous, and include density dependence 6 , weather conditions 7 that affect food availability 3 , predation rates 8 , and land use change 9,10 , with the importance of these drivers varying across systems . Given the near ubiquity of rodents and the diverse ecological roles they play as consumers, prey, and reservoirs for parasites and pathogens, these fluctuations are consequential for many ecological processes, including the transmission of zoonotic pathogens . Zoonotic diseases caused by these pathogens are an increasing threat to human health and welfare 16 , yet despite our increasing understanding of ecological factors that contribute to outbreaks, our ability to predict zoonotic spillover transmission remains limited. Rodents host a greater diversity of zoonotic pathogens than other mammal orders 17 and, together with bats and primates, they harbour the majority of zoonotic viruses 18 . Within rodents, species with fast life history strategies (e.g., early and frequent reproduction) appear disproportionately likely to act as zoonotic reservoirs , but the mechanisms underlying the effects of life history on reservoir status are poorly understood, as are the pathways leading to direct or indirect contact between rodents and humans 18 -a necessary condition for the transmission of many rodent-borne zoonoses. The propensity of some rodent species to live exclusively or occasionally in or near human dwellings (synanthropy) has long been acknowledged to increase transmission risk of important zoonoses threatening public health. Synanthropic behaviour and close human contact with globally distributed rodents like the house rat (Rattus rattus), brown rat (Rattus norvegicus) and house mouse (Mus musculus) have been linked to numerous zoonoses, including plague and

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