Population fluctuations and synanthropy explain transmission risk in rodent-borne zoonoses

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.

Fig. 1. Pathways increasing transmission risk from rodent-borne pathogens.

a, b Contact between rodents and humans increases transmission risk; a either with rodents moving into human dwellings and environments or with b, humans moving into rodent habitats or using rodents as a natural resource. c Factors (green boxes) and associated key traits of mechanisms (arrows) explaining increased transmission risk from rodent-borne pathogens. Description of mechanisms: Body mass as a key life history trait can dichotomously increase transmission risk. While rodents with high body mass are frequently hunted for fur or meat, many rodents with low body mass have less developed immune defence strategies and exhibit large population fluctuations (high s-index) resulting in population outbreaks. Periods of high rodent population density are frequently associated with abundant dispersal into human-dominated environments. As pathogens are frequently associated with synanthropic and habitat generalist rodents, these rodents increase transmission risk via proximity to humans. Being a reservoir poses an apparent transmission risk. In the light of many rodent-borne pathogens still being undetected, factors like synanthropy, habitat generalism, high population fluctuations and/or high body mass are important predictors of transmission risk.

Fig. 2. Predictors of reservoir status.

Final structural equation model linking reservoir status of rodent species (n = 269) with their synanthropy and hunting status, population fluctuations (s-index, log-transformed), and adult body mass, controlling for their occurrence in a range of habitats and the number of studies available per species. One-sided (directional) arrows represent a causal influence originating from the variable at the base of the arrow, with the width of the arrow and associated value representing the standardised strength of the relationship. The small double-sided arrows and numbers next to each response (endogenous) variable represent the error variance.

Fig. 3. Characteristics of reservoir and synanthropic rodents.

a Reservoir rodents are predominately synanthropic (n = 436 with n (non-reservoir) = 154, n (reservoir) = 282). b Synanthropic rodents display high population fluctuations (high s-index) (n = 269) and c, occur in multiple artificial habitats (n = 269) (Tables 1–3). In a, estimated probability and 95% confidence intervals are shown and in b–c, estimated probability is shown and shaded areas show 95 % confidence intervals.

Fig. 4. Habitat types occupied by rodents.

a Percentage of non-reservoir (black bars; n = 154) and reservoir rodents (red bars; n = 282), respectively, occurring in natural and artificial (shaded) habitats. b Habitat generalism of reservoir rodents. Reservoir rodents occurring in natural habitats potentially move into artificial habitats, e.g., during periods of high population density or when natural habitat is degraded. Thickness of curves represents number of rodents shared between natural and artificial habitat.

Fig. 5. Global distribution of the number of rodent species by category.

a All rodent species (n = 2308), b reservoir rodents (n = 282), c ratio between the number of reservoir and total number of rodents, d rodents occurring in artificial habitats (n = 186), e synanthropic rodents (n = 155), f rodents exhibiting pronounced population fluctuations (s-index >0.3, Methods; n = 159), g hunted rodents (n = 83). Warmer colours highlight areas of high species richness. See Methods for image licensing.