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Extremely Low Prevalence of Batrachochytrium dendrobatidis in Frog Populations from Neotropical Dry Forest of Costa Rica Supports the Existence of a Climatic Refuge from Disease

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Abstract

Population declines and extinctions of numerous species of amphibians, especially stream-breeding frogs, have been linked to the emerging infectious disease chytridiomycosis, caused by the chytrid fungus, Batrachochytrium dendrobatidis. In Central America, most of the 34 species of the Craugastor punctariolus species group have disappeared in recent years in high- and low-elevation rainforests. Distribution models for B. dendrobatidis and the continuous presence of the extirpated stream-dwelling species, Craugastor ranoides, in the driest site of Costa Rica (Santa Elena Peninsula), suggest that environmental conditions might restrict the growth and development of B. dendrobatidis, existing as a refuge from chytridiomycosis-driven extinction. We conducted field surveys to detect and quantify the pathogen using Real-time PCR in samples from 15 species of frogs in two locations of tropical dry forest. In Santa Elena Peninsula, we swabbed 310 frogs, and only one sample of the species, C. ranoides, tested positive for B. dendrobatidis (prevalence <0.1%). In Santa Rosa Station, we swabbed 100 frogs, and nine samples from three species tested positive (prevalence = 9.0%). We failed to detect signs of chytridiomycosis in any of the 410 sampled frogs, and low quantities of genetic equivalents (between 0 and 1073) were obtained from the ten positive samples. The difference in the prevalence between locations might be due not only to the hotter and drier conditions of Santa Elena Peninsula but also to the different compositions of species in both locations. Our results suggest that B. dendrobatidis is at the edge of its distribution in these dry and hot environments of tropical dry forest. This study supports the existence of climatic refuges from chytridiomycosis and highlights the importance of tropical dry forest conservation for amphibians in the face of epidemic disease.

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Acknowledgements

This study was supported by Consejo Nacional de Ciencia y Tecnología (CONICIT) grant FI-113-07 and the Sistema de Estudios de Posgrado at the Universidad de Costa Rica (SEP-UCR). We thank Roger Blanco and María Marta Chavarría for their support throughout this project. We also thank Sandra Silva and Rebeca Campos at Centro de Investigaciones en Biología Celular y Molecular (CIBCM) for allowing use of their laboratories and facilities, and Margarita Lampo at Instituto Venezolano de Investigaciones Científicas (IVIC) for the donation of the B. dendrobatidis solution standards. We are grateful to the Research and Analysis Network for Neotropical Amphibians (RANA) for the Quantitative PCR training course. Thanks are also due to Joseph Mendelson III and Gilbert Barrantes for discussions and reviews of earlier drafts. This study was conducted under permit #ACG-PI-037-2007 of Ministerio de Ambiente y Energía (MINAE).

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Zumbado-Ulate, H., Bolaños, F., Gutiérrez-Espeleta, G. et al. Extremely Low Prevalence of Batrachochytrium dendrobatidis in Frog Populations from Neotropical Dry Forest of Costa Rica Supports the Existence of a Climatic Refuge from Disease. EcoHealth 11, 593–602 (2014). https://doi.org/10.1007/s10393-014-0967-2

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