A shared pathogen reservoir can tip widespread infection into mass mortality
Abstract
Pathogens that persist subclinically across many wildlife populations can drive mass mortality in others. Mass mortality is often abrupt, and the timing can be difficult to predict from host or habitat features alone. In a recent field study tracking ranavirus epizootics in wood frog (Rana sylvatica) breeding ponds, we found that no environmental or biotic feature reliably predicted die-off occurrence or timing. Instead, the trajectory of viral accumulation in the water column was the strongest dynamic predictor of mass mortality. Infected hosts shed virus throughout epizootics, but the influence of waterborne viral concentration on disease progression was apparent only near die-off onset. This pattern suggests a potential threshold-dependent feedback operating through the shared viral environment. Here, we develop a compartmental model linking waterborne viral concentration to the rate at which subclinical infections progress to clinical, high-shedding states within already-infected hosts. We show that a dose-dependent progression model generates the two-phase epizootic trajectory observed in natural die-offs: prolonged subclinical circulation followed by abrupt clinical transition after environmental virus crosses an escalation threshold. The model exhibits a sharp phase transition between subclinical circulation and mass mortality, governed mainly by the clinical-to-subclinical shedding ratio, host density, and pond volume. Existing explanations for die-off variation emphasize individual-level susceptibility, but our model demonstrates that dose-dependent environmental feedback, a mechanism not previously formalized at the population level, can generate the transition from subclinical infection to mass mortality without invoking individual variation in host susceptibility. This mechanism may apply in any system where hosts share a bounded environment, pathogen dose influences disease severity, and pathogen shedding increases with disease progression.
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