Widespread Pig Farming Practice Linked to Shifts in Skin Microbiomes and Disease in Pond-Breeding Amphibians

Abstract

Farming practices may reshape the structure of watersheds, water quality, and the health of aquatic organisms. Nutrient enrichment from agricultural pollution increases disease pressure in many host-pathogen systems, but the mechanisms underlying this pattern are not always resolved. For example, nutrient enrichment should strongly influence pools of aquatic environmental bacteria, which has the potential to alter microbiome composition of aquatic animals and their vulnerability to disease. However, shifts in the host microbiome have received little attention as a link between nutrient enrichment and diseases of aquatic organisms. We examined nutrient enrichment through the widespread practice of integrated pig-fish farming and its effects on microbiome composition of Brazilian amphibians and prevalence of the globally distributed amphibian skin pathogen Batrachochytrium dendrobatidis (Bd). This farming system drove surges in fecal coliform bacteria, disturbing amphibian skin bacterial communities such that hosts recruited higher proportions of Bd-facilitative bacteria and carried higher Bd prevalence. Our results highlight previously overlooked connections between global trends in land use change, microbiome dysbiosis, and wildlife disease. These interactions may be particularly important for disease management in the tropics, a region with both high biodiversity and continually intensifying anthropogenic pressures on aquatic wildlife habitats.