Diversity loss and disease emergence: Insights from amphibian malformations and parasite infection

Global increases in the emergence of human and wildlife diseases underscore the urgent need to develop a broader ecological understanding of host-parasite-environment interactions.  Hypothesized linkages between biodiversity losses and increased pathogen transmission have been advanced to explain the emergence of some diseases; however, experimental research to identify the mechanisms behind this relationship has largely been lacking.  Here we experimentally investigated how changes in amphibian communities affected the transmission and pathology of a trematode parasite (Ribeiroia ondatrae), which has been identified as a widespread cause of severe limb malformations.  We raised larval American toads (B. americanus) either individually, paired with a second larval toad, or paired with a larval grey treefrog (H. versicolor).  During early limb development, Ribeiroia cercariae were added to half of the containers and allowed to infect developing larvae.  Exposure to Ribeiroia significantly enhanced mortality (15%) and malformation (40%) levels in metamorphosing toads while delaying time-to-metamorphosis.  Parasite infection had no effect on survival or limb development among grey treefrogs, but competition with H. versicolor  caused delyaed development and reduced metamorphic size in co-occurring toads.  Intriguingly, however, parasite-exposed toads raised with H. versicolor exhibited fewer malformations and higher survival than toads raised in isolation or with other toads.  Correspondingly, the presence of H. versicolor significantly reduced the level of Ribeiroia infection among co-occurring toads and the total number of recovered parasites (sum of two animals).  Our results suggest that, owing to interspecific variation in immune function, multi-species amphibian communities may inhibit trematode parasite transmission and reduce infection-mediated pathology and mortality.