The Lethal Fungus Batrachochytrium dendrobatidis Is Present in Lowland Tropical Forests of Far Eastern Panamá

et al. (2014) The Lethal Fungus Batrachochytrium dendrobatidis Is Present in Lowland Tropical Forests of Far Eastern Panama. PLoS ONE 9(4): e95484. doi:10.1371/journal.pone.0095484 The Lethal Fungus Batrachochytrium dendrobatidis Is Present in Lowland Tropical Forests of Far Eastern Panama Eria A. Rebollar 0 Myra C. Hughey 0 Reid N. Harris 0 Rickie J. Domangue 0 Daniel Medina 0 Roberto Iba n ez 0 Lisa K. Belden 0 Ilse D. Jacobsen, Leibniz Institute for Natural Products Research and Infection Biology- Hans Knoell Institute, Germany 0 1 Department of Biology, James Madison University , Harrisonburg , Virginia, United States of America, 2 Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, United States of America, 3 Department of Mathematics and Statistics, James Madison University , Harrisonburg , Virginia, United States of America, 4 Smithsonian Tropical Research Institute , Balboa, Anco n , Republic of Panama The fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), is one of the main causes of amphibian population declines and extinctions all over the world. In the Neotropics, this fungal disease has caused catastrophic declines in the highlands as it has spread throughout Central America down to Panama . In this study, we determined the prevalence and intensity of Bd infection in three species of frogs in one highland and four lowland tropical forests, including two lowland regions in eastern Panama in which the pathogen had not been detected previously. Bd was present in all the sites sampled with a prevalence ranging from 15-34%, similar to other Neotropical lowland sites. The intensity of Bd infection on individual frogs was low, ranging from average values of 0.11-24 zoospore equivalents per site. Our work indicates that Bd is present in anuran communities in lowland Panama , including the Darie n province, and that the intensity of the infection may vary among species from different habitats and with different life histories. The population-level consequences of Bd infection in amphibian communities from the lowlands remain to be determined. Detailed studies of amphibian species from the lowlands will be essential to determine the reason why these species are persisting despite the presence of the pathogen. - Funding: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This project was funded by the National Science Foundation Dimensions of Biodiversity program, under grants DEB-1136640 to Lisa K. Belden and DEB-1136602 to Reid N. Harris (http://www. nsf.gov/). Competing Interests: The authors have declared that no competing interests exist. Habitat loss and overexploitation are two of the main causes of biodiversity loss on the planet [1]. Amphibians are also threatened by chytridiomycosis [2,3], an infectious disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd). In recent decades, more than 40% of amphibian species have become vulnerable to extinction [1], and Bd has been detected in at least 48% of the amphibian species studied worldwide [4,5]. In the tropics, drastic amphibian declines in forested protected areas have been clearly associated with chytridiomycosis [6,7]. In the Neotropics, dramatic amphibian declines associated with Bd infection have been extensively documented in highland forests [6,8,9,10] where the greatest losses in species diversity and population abundance in response to establishment of the pathogen have been described [11]. Moreover, a wave of infection spreading from Mexico down through Central America to Panama has been thoroughly described [12,13,14]. In addition, Bd infection has been spreading across highland forests in South America including the Colombian Andes [15,16,17]. Thus, the Darien region of Panama and Colombia is considered one of the last Bd nave areas in Central America. Although invasion of Bd was thought to be inevitable, no surveys before this study have confirmed the presence of the pathogen into this region. However, in 2010, two frogs out of 93 individuals were infected with Bd in Tort, a site at the Panama Province close to the Darien [18]. Bd has been detected in lowland forests [10,13,1922]; however, in low elevation sites there is little evidence of population declines associated with Bd [20]. One of the possible reasons for the absence of dramatic declines in the lowlands is that environmental conditions, such as temperature and moisture, are not optimal for Bd growth and successful colonization [23,24,25]. In addition, it is possible that lowland species are less susceptible to infection because of physiological and ecological traits, such as differential immune response, production of antimicrobial peptides, presence of symbiotic beneficial bacterial, behavioral patterns and habitat associations [19,2629]. Overall, the study of amphibian species persisting in the lowlands with Bd is a key component to understanding the nature of the disease, as well as how this pathogen spreads and colonizes new areas and hosts. In this study, we determined the prevalence and intensity of Bd infection in three species of frogs from the tropical forests of Panama. These amphibian species, Agalychnis callidryas, Dendropsophus ebraccatus, and Craugastor fitzingeri, are common in the lowlands, although their habitat distribution reaches highland forest up to 8201520 m [30,31]. A. callidryas and D. ebraccatus are nocturnal treefrogs (family: Hylidae) that spend most of the time in the forest canopy except for the breeding season, when individuals can be found on low vegetation near ponds; whereas C. fitzingeri (family: Craugastoridae) is mainly a nocturnal and terrestrial species usually found in the leaf litter and also along the margins of streams. The two treefrogs are pond breeders with arboreal eggs and aquatic larvae, whereas C. fitzingeri is a direct developer. Previous studies have determined that Bd prevalence and infection intensity can vary between species from different habitats and with different life histories. For instance, Bd prevalence tends to be higher in frogs from riparian habitats than in frogs from terrestrial habitats [19], and breeding habitats can be important predictors of infection intensity [22,32,33]. Based on the contrasting life histories, we hypothesized that Bd infection, if present, could have different patterns among the three frog species that we studied. We propose two contrasting scenarios; in the first C. fitzingeri may have less exposure to Bd since all life stages of this frog are terrestrial, whereas the treefrogs A. callidryas and D. ebraccatus have an aquatic tadpole stage during which they may have more exposure to the aquatic zoospores of Bd [28]. Therefore, we would expect C. fitzingeri to have lower prevalence and intensity of infection in contrast to the treefrogs. Alternatively, it is likely that the treefrogs habitat as a (...truncated)