Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America.

Tara Chestnut,Chauncey Anderson,Deanna H Olson,Mary Voytek,Andrew R Blaustein,Radu Popa,Julie Kirshtein,Benedikt R Schmidt

doi:10.1371/journal.pone.0106790

Abstract

Biodiversity losses are occurring worldwide due to a combination of stressors. For example, by one estimate, 40% of amphibian species are vulnerable to extinction, and disease is one threat to amphibian populations. The emerging infectious disease chytridiomycosis, caused by the aquatic fungus Batrachochytrium dendrobatidis (Bd), is a contributor to amphibian declines worldwide. Bd research has focused on the dynamics of the pathogen in its amphibian hosts, with little emphasis on investigating the dynamics of free-living Bd. Therefore, we investigated patterns of Bd occupancy and density in amphibian habitats using occupancy models, powerful tools for estimating site occupancy and detection probability. Occupancy models have been used to investigate diseases where the focus was on pathogen occurrence in the host. We applied occupancy models to investigate free-living Bd in North American surface waters to determine Bd seasonality, relationships between Bd site occupancy and habitat attributes, and probability of detection from water samples as a function of the number of samples, sample volume, and water quality. We also report on the temporal patterns of Bd density from a 4-year case study of a Bd-positive wetland. We provide evidence that Bd occurs in the environment year-round. Bd exhibited temporal and spatial heterogeneity in density, but did not exhibit seasonality in occupancy. Bd was detected in all months, typically at less than 100 zoospores L−1. The highest density observed was ∼3 million zoospores L−1. We detected Bd in 47% of sites sampled, but estimated that Bd occupied 61% of sites, highlighting the importance of accounting for imperfect detection. When Bd was present, there was a 95% chance of detecting it with four samples of 600 ml of water or five samples of 60 mL. Our findings provide important baseline information to advance the study of Bd disease ecology, and advance our understanding of amphibian exposure to free-living Bd in aquatic habitats over time.

Highlights

Loss of biodiversity in terrestrial, freshwater, and marine systems is occurring at a global scale [1,2,3,4,5]
Our findings address important baseline information to advance the study of Batrachochytrium dendrobatidis (Bd) disease ecology in temperate-zone systems, and to advance our understanding of the likelihood of amphibian exposure to free-living Bd in aquatic habitats over time
Bd density was highest in spring (Figures 2 & 3), and at two Nevada sites sampled in May, Bd densities were more than 50 times the densities that we observed at other sites (2,109 and 4,924 zoospores L21)

Summary

Introduction

Loss of biodiversity in terrestrial, freshwater, and marine systems is occurring at a global scale [1,2,3,4,5]. The causes of losses are often complex and include synergistic effects of natural and human-induced stressors, such as habitat loss and fragmentation [6,7], urbanization [8], invasive species [7,9,10], contaminants [11,12,13], global climate change [14,15,16], and emerging infectious diseases [17,18]. In the last 35 years, one estimate suggests that the amphibian extinction rate is at least 105 times higher than the expected rate [19], with 32.5 to 41% of amphibian species threatened [7,20]. Chytridiomycosis, the emerging infectious disease caused by the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), is implicated as a causal agent in many recent global amphibian population declines and extinctions [34,35,36]

Methods

Results

Conclusion