Abstract
Emerging infectious diseases are a growing threat to biodiversity worldwide. Outbreaks of the infectious disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), are implicated in the decline and extinction of numerous amphibian species. In Costa Rica, a major decline event occurred in 1987, more than two decades before this pathogen was discovered. The loss of many species in Costa Rica is assumed to be due to Bd-epizootics, but there are few studies that provide data from amphibians in the time leading up to the proposed epizootics. In this study, we provide new data on Bd infection rates of amphibians collected throughout Costa Rica, in the decades prior to the epizootics. We used a quantitative PCR assay to test for Bd presence in 1016 anuran museum specimens collected throughout Costa Rica. The earliest specimen that tested positive for Bd was collected in 1964. Across all time periods, we found an overall infection rate (defined as the proportion of Bd-positive individuals) of 4%. The number of infected individuals remained relatively low across all species tested and the range of Bd-positive specimens was shown to be geographically constrained up until the 1980s; when epizootics are hypothesized to have occurred. After that time, infection rate increased three-fold, and the range of specimens tested positive for Bd increased, with Bd-positive specimens collected across the entire country. Our results suggest that Bd dynamics in Costa Rica are more complicated than previously thought. The discovery of Bd’s presence in the country preceding massive declines leads to a number of different hypotheses: 1) Bd invaded Costa Rica earlier than previously known, and spread more slowly than previously reported; 2) Bd invaded multiple times and faded out; 3) an endemic Bd lineage existed; 4) an earlier Bd lineage evolved into the current Bd lineage or hybridized with an invasive lineage; or 5) an earlier Bd lineage went extinct and a new invasion event occurred causing epizootics. To help visualize areas where future studies should take place, we provide a Bd habitat suitability model trained with local data. Studies that provide information on genetic lineages of Bd are needed to determine the most plausible spatial-temporal, host-pathogen dynamics that could best explain the epizootics resulting in amphibian declines in Costa Rica and throughout Central America.
Highlights
Amphibians are experiencing a global extinction event [1,2]
Batrachochytrium dendrobatidis (Bd) became more common throughout the country in the late 1980s and 1990s (Figs 1A and 2); conclusions derived from the presence of Bd based on museum specimens that were not collected for disease studies are limited
Our retrospective study using museum specimens revealed that Bd was present in Costa Rica at least two decades before declines were discovered at Monteverde [20], and four decades before Bd was described
Summary
Amphibians are experiencing a global extinction event [1,2]. Though many factors contribute to population declines, the emergence of the fungal pathogen Batrachochytrium dendrobatidis (Bd) is one of the most important [3]. The disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (hereafter Bd), was first described in 1999 and has since been found all over the world [3,4,5]. Bd is composed of many genetic lineages that vary in virulence and affect host species differently. The panzootic disease is attributed to Bd-GPL, a Global Panzootic Lineage of Bd associated with Bd epizootics and host population collapse [6]. Other lineages of Bd have been shown to be less virulent and have been identified in areas lacking epizootics [7]. Bd infects the skin of the amphibian and causes hyperkeratosis, the thickening of skin which disrupts the amphibian’s osmotic balance; leading to death by cardiac arrest in highly infected individuals [8,9]
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