Culling the sick and the young: How predators, resources, and stage structure interact to spread disease in hosts

Background/Question/Methods

The “healthy herds” hypothesis says that predators that selectively cull infected hosts can reduce disease prevalence in host populations.  Such connections between predators and epidemiology suggest exciting opportunities to control disease with top-down community ecology.  However, many predators also selectively cull juvenile hosts.  Here, we explore the possibility that such stage-structured preference of predators could actually spread disease.  Consider our focal case study of disease in the plankton.  In both Michigan and Indiana, we have shown that lakes with higher densities of the invertebrate predator Chaoborus spp. have larger epidemics of a virulent fungus (Metschnikowia bicuspidata) in populations of the zooplankton host (Daphnia dentifera), an important grazer on phytoplankton.  This predator also selectively preys upon juvenile hosts.  Adult hosts, meanwhile, are much more susceptible to the fungus (because they are bigger). Motivated and inspired by this natural history, we analyze at set of mathematical models that incorporate various assumptions about epidemiology of the host-parasite interaction, a stage-structured host, and possible competitive interactions between juvenile and adult hosts for a dynamic resource. 

Results/Conclusions

We found that predators that selectively prey on juvenile hosts can either inhibit disease or enhance it, depending on feedbacks involving stage structure and resource competition.  The simplest scenarios consider a host with fixed development time between the juvenile and adult stages.  In these cases, the predator decreases three key disease indices – invasion success of the parasite (R0), infection prevalence, and density of infected hosts – especially when these predators preferentially cull infected hosts.  If juveniles consume environmental-distributed infectious stages of the parasite (e.g., spores), culling the young can enhance parasite invasion but still reduces disease prevalence.  However, if development time depends on resource abundance that itself depends on density of hosts, then culling the young can enhance all of the disease indices.  Now, culling the young elevates resource density, thereby accelerating development time of juveniles into adults (who are more susceptible).  More adults then enhance disease spread – especially when juveniles consume infectious stages without becoming sick.  These effects can operate even when predators selectively cull infected hosts.  Thus, predators can spread disease when top-down and bottom-up forces act simultaneously on stage-structured hosts and parasites.  Such results illustrate the power of taking a community ecology approach to studying disease.