Hunting, host longevity, and pathogen dynamics in a Madagascar fruit bat community

Background/Question/Methods

In light of the ongoing West African Ebola epidemic, the role of bats as reservoirs for highly virulent zoonotic pathogens is receiving increasing attention. An ecological understanding of the mechanisms motivating epidemic spikes in transmission among bat reservoirs for infection will be essential to predicting and preventing future incidence of bat-borne pathogen spillover. Previous theoretical and experimental work demonstrates that anthropogenic culling of natural pathogen reservoirs can potentially elevate pathogen prevalence (and corresponding zoonotic risk) by relaxing natural density-dependent regulation on host births, opening niche space for migration of susceptible young, or enabling establishment of less virulent pathogen strains. We explore the impacts of human hunting on host longevity and implications for pathogen dynamics among fruit bats consumed as bushmeat in the Madagascar ecosystem.

Specifically, we model age-structured equilibrium dynamics for a directly-transmitted virus, then explore how heterogeneous harvesting across these age classes might alter abundance and age-structure, perhaps elevating spillover risk. We derive our model parameters from a combination of interview data collected from Malagasy bushmeat hunters and empirical field data documenting age-structured coronavirus prevalence in two Malagasy fruit bats, Pteropus rufus and Eidolon dupreanum. We use cementum annuli analysis of extracted tooth samples collected from live bats under anaesthesia to estimate age. 

Results/Conclusions

A comparison in age estimates extracted from tooth samples in both the modern and subfossil records demonstrates a substantial reduction in fruit bat lifespan corresponding to the timing of human arrival to Madagascar; we hypothesize this longevity truncation to be the result of intensive bushmeat hunting across older age classes of Malagasy fruit bat. Our preliminary age-prevalence estimates for coronavirus infection in Malagasy bats suggest that these older age classes are largely composed of individuals that have already experienced infection, mounted immune responses, and cleared the pathogen under consideration. Correspondingly, we class these individuals as “Recovered” in a traditional Susceptible-Infected-Recovered (SIR) compartmental model. Our theoretical analysis demonstrates that targeted hunting of recovered individuals will ultimately result in higher population-wide prevalence of infected individuals, which may elevate risks for zoonotic spillover. Our study offers evidence of the disease-exacerbating consequences of culling of reservoir populations for zoonotic pathogens. We advocate for fruit bat conservation measures that offer an opportunity to synergistically benefit both hunting-threatened wildlife populations and human public health.