Pathways of amphibian chytrid fungus dispersal: global biosecurity and conservation implications

Abstract

Spread of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) poses the greatest emerging threat to global amphibian biodiversity. Bd's low host species specificity allows the disease it causes — chytridiomycosis — to affect many of the 7,000 species of amphibians and drive population declines and extinctions worldwide. Although discovered nearly 20 years ago, the origin of Bd and catalyst of the seemingly recent global disease event remain obscure. Today, this international epizootic continues to advance virtually uncontrolled. Modes of global Bd dispersal are not well understood, hampering the development and implementation of targeted biosecurity efforts to reduce spread. Bd is an aquatic pathogen most often associated with amphibian species that live in or near permanent bodies of water. It can neither survive desiccation nor extended exposure to elevated temperatures, but few environmental barriers appear to impede the spread of Bd. It has crossed oceans, infected terrestrial direct-developing amphibians that do not live in water, and been introduced to every continent (except Antarctica). Although low densities of Bd have been found in the environment outside of a host, amphibians consistently carry the highest pathogen loads and appear to be the primary host organisms that vector Bd. The international trade in live amphibians transports millions of animals annually. Most previous research has focused on this anthropogenic activity as the primary pathway of global Bd dispersal. This is a sensible assumption—the highly visible movement of Bd hosts together with the lack of disease control suggests that Bd-positive animals are commonly transported in these shipments. Unfortunately, all previous surveillance efforts that aimed to demonstrate this phenomenon were performed in animal markets in Bd-positive countries where contamination from domestic Bd could not be excluded as a potential source of infection. Upon close examination of global Bd distribution patterns, I found that regions of Bd presence do not exclusively overlap those of notable amphibian trade, raising questions as to the sources and pathways involved in pathogen dispersal. For instance, despite the absence of commercial amphibian importation to the islands of Dominica and Montserrat, chytridiomycosis drove the near-extinction of the Mountain Chicken frog (Leptodactylus fallax). Likewise, chytridiomycosis emerged in remote wilderness areas in Central America and Australia, again with no clear link to amphibian trade activity. Thus, despite the similar absence of commercial amphibian importation in Madagascar, it seems unlikely that this alone prevents the introduction of Bd. Meanwhile despite intensive field and market surveillance in Hong Kong — a global amphibian trade hub — Bd has neither been detected nor have amphibian declines been observed. Therefore, I hypothesized that additional pathways of Bd dispersal exist in the absence of commercial amphibian trade that can also transport this pathogen global distances. The…