Human activities such as agriculture can create abundant and predictable food subsidies to wildlife that induce long-term changes in behavior and physiology. These changes in turn can alter infectious disease dynamics. Specifically, prior work predicts that how anthropogenic food affects wildlife immune defense can determine whether provisioning amplifies or dampens pathogen transmission. We tested relationships between resource provisioning and immune function through a cross-sectional study of 275 vampire bats (Desmodus rotundus) across 16 sites in the rainforests of Peru and Belize that differ in the availability of livestock, an important food source for vampire bats in agricultural and human-modified landscapes. We predicted that livestock expansion could reduce starvation stress and energy spent foraging, allowing bats to invest more in costly immune defenses such as antibody response and in turn resist rabies infection. We quantified the proportion of lymphocytes in blood smears and levels of immunoglobulin G in serum and tested for differential immunity as a function of livestock density. We next used weighted nonlinear least squares to fit different functional responses of immune parameters to livestock density. Resource-dependent immune function was then integrated into a compartmental model of rabies transmission in vampire bats to simulate how resource provisioning could affect the basic reproductive number (R0).
Results/Conclusions
Contrary to our predictions, our data suggest that livestock expansion into jungle habitats is associated with impaired immune function. Vampire bats from high-livestock habitats had fewer lymphocytes in blood and lower levels of immunoglobulin G in serum. Integrating resource dependence into the probability of resisting rabies infection into an analytic expression for R0 showed that rabies virus invasion (R0 > 1) can become more likely at intermediate and high livestock densities. Therefore livestock expansion could possibly sustain rabies transmission within a bat colony even in the absence of immigration of rabid bats, shown in prior models as necessary for viral persistence. Together these empirical findings and simulations illustrate that anthropogenic provisioning of wildlife can enhance pathogen transmission through a paradoxical mechanism of reducing immune performance. Furthermore, we here provide a foundation for integrating additional forms of resource dependence (i.e., spatial dynamics and host movement) into mathematical models of infectious disease.