The application of community ecology theory to co-infections in wildlife hosts

Abstract

Priority effect theory, a foundational concept from community ecology, states that the order and timing of species arrival during species assembly can affect species composition. Although this theory has been applied to co-infecting parasite species, it has almost always been with a single time lag between co-infecting parasites. Thus, how the timing of parasite species arrival affects co-infections and disease remains poorly understood. To address this gap in the literature, we exposed post-metamorphic Cuban tree frogs (Osteopilus septentrionalis) to Ranavirus, the fungus Batrachochytrium dendrobatidis (Bd), a nematode Aplectana hamatospicula, or pairs of these parasites either simultaneously or sequentially at a range of time lags and quantified load of the secondary parasite and host growth, survival and parasite tolerance. Prior exposure to Bd or A. hamatospicula significantly increased viral loads relative to hosts singly infected with Ranavirus, whereas A. hamatospicula loads in hosts were higher when co-exposed to Bd than when co-exposed to Ranavirus. There was a significant positive relationship between time since Ranavirus infection and Bd load, and prior exposure to A. hamatospicula decreased Bd loads compared to simultaneous co-infection with these parasites. Infections with Bd and Ranavirus either singly or in co-infections decreased host growth and survival. This research reveals that time lags between co-infections can affect parasite loads, in line with priority effects theory. As co-infections in the field are unlikely to be simultaneous, an understanding of when co-infections are impacted by time lags between parasite exposures may play a major role in controlling problematic co-infections.