Identity and density of parasite exposures alter the outcome of coinfections: Implications for management

Although research has focused on density-dependent responses of hosts to single-parasite infections, hosts are exposed to numerous parasites simultaneously under natural conditions and if these exposures lead to infections, they can threaten host populations and ecosystem stability. Moreover, spatiotemporal variation in abundance of co-occurring parasites might influence host infection intensity. If interactions are consistent between different coinfecting parasites, then these patterns could give managers another tool to control disease spread and even predict problematic disease emergences. We investigated how parasite density and identity alter within-host coinfection dynamics. To test this, we simultaneously exposed Cuban treefrogs Osteopilus septentrionalis as a model amphibian species to all pairwise combinations of three problematic parasites that commonly coinfect amphibians: the fungus Batrachochytrium dendrobatidis (Bd), the nematode Aplectana hamatospicula and Ranavirus. Hosts were exposed to one parasite at a fixed dose and another parasite at a range of five doses. Higher doses of Bd decreased Ranaviral and A. hamatospicula loads, but Bd load was not influenced by the dose of either parasite. Ranaviral load was negatively associated with A. hamatospicula dose, but A. hamatospicula load was not affected by Ranaviral dose. We found that all the pairwise coinfections were dependent on parasite density and that pairwise interactions were highly asymmetric-strong in one direction and weak in the other-consistent with interactions dominating food webs. Synthesis and applications: We also revealed that the exposure dose of A. hamatospicula was positively associated with host tolerance to Bd infection and negatively associated with Ranaviral load in hosts. Ranavirus and Bd cause mass die-offs in amphibians, but A. hamatospicula does not. Therefore, in systems where these parasites coexist, maintaining or increasing densities of A. hamatospicula could reduce the negative effects of Bd and Ranavirus infections. Additionally, if these asymmetric and density-dependent patterns from community ecology are applicable to other amphibian coinfections or coinfections in other systems, this should allow conservation organizations and resource managers to predict outbreaks and manage host declines associated with deadly parasites by modifying the abundance of coinfecting parasites that might be easier to manage.