Contributed Paper Batrachochytrium dendrobatidis and the Collapse of Anuran Species Richness and Abundance in the Upper Manu National Park, Southeastern Peru ALESSANDRO CATENAZZI,��� EDGAR LEHR,��� LILY O. RODRIGUEZ,��� AND VANCE T. VREDENBURG�� ���Department of Integrative Biology, University of California at Berkeley, 3060 Valley Life Sciences Building, Berkeley, CA 94720, U.S.A, email acatenazzi@gmail.com ���Department of Biology, Illinois Wesleyan University, 303 East Emerson, Bloomington, IL 61701, U.S.A. ���GTZ-Per�� u, Los Incas 172, San Isidro, Lima 34, Peru ��Department of Biology, San Francisco State University, San Francisco, CA 94132, U.S.A. Abstract: Amphibians are declining worldwide, but these declines have been particularly dramatic in tropi- cal mountains, where high endemism and vulnerability to an introduced fungal pathogen, Batrachochytrium dendrobatidis (Bd), is associated with amphibian extinctions. We surveyed frogs in the Peruvian Andes in mon- tane forests along a steep elevational gradient (1200���3700 m). We used visual encounter surveys to sample stream-dwelling and arboreal species and leaf-litter plots to sample terrestrial-breeding species. We compared species richness and abundance among the wet seasons of 1999, 2008, and 2009. Despite similar sampling effort among years, the number of species (46 in 1999) declined by 47% between 1999 and 2008 and by 38% between 1999 and 2009. When we combined the number of species we found in 2008 and 2009, the decline from 1999 was 36%. Declines of stream-dwelling and arboreal species (a reduction in species richness of 55%) were much greater than declines of terrestrial-breeding species (reduction of 20% in 2008 and 24% in 2009). Similarly, abundances of stream-dwelling and arboreal frogs were lower in the combined 2008���2009 period than in 1999, whereas densities of frogs in leaf-litter plots did not differ among survey years. These declines may be associated with the infection of frogs with Bd. B. dendrobatidis prevalence correlated significantly with the proportion of species that were absent from the 2008 and 2009 surveys along the elevational gradient. Our results suggest Bd may have arrived at the site between 1999 and 2007, which is consistent with the hypothesis that this pathogen is spreading in epidemic waves along the Andean cordilleras. Our results also indicate a rapid decline of frog species richness and abundance in our study area, a national park that contains many endemic amphibian species and is high in amphibian species richness. Keywords: amphibians, elevational gradient, extinction, montane forest, Neotropics, threatened species, trop- ical Andes Batrachochytrium dendrobatidis y el Colapso de la Riqueza de Especies y Abundancia de Anuros en el Parque Nacional del Manu, Sureste de Per�� u Resumen: Las poblaciones de anfibios est�� an disminuyendo mundialmente, pero estas disminuciones han sido particularmente dramaticas �� en monta�� nas tropicales, donde el endemismo y la vulnerabilidad a un patogeno �� fungico �� introducido, Batrachochytrium dendrobatidis (Bd), est�� an asociados con extinciones de an- fibios. Muestreamos ranas en el los Andes Peruanos en bosques montanos a lo largo de un gradiente altitudinal pronunciado (1200���3700 m). Utilizamos t�� ecnicas de encuentros visuales para muestrear especies arboreas�� Paper submitted May 7, 2010 revised manuscript accepted June 22, 2010. 1 Conservation Biology, Volume **, No. **, ***���*** C 2010 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2010.01604.x

2 Frog Declines in the Tropical Andes y en quebradas y cuadrantes en la hojarasca para muestrear especies terrestres. Comparamos la riqueza de especies y la abundancia entre las estaciones lluviosas de 1999, 2008 y 2009. No obstante esfuerzos de muestreo similares, el numero �� de especies (46 en 1999) disminuy�� o en 47% entre 1999 y 2008 y en 38% entre 1999 y 2009. Cuando combinamos el numero �� de especies encontradas en 2008 y 2009, la disminuci�� on desde 1999 fue de 36%. Las disminuciones de especies arboreas �� y que se reproducen en quebradas (una reducci�� on de 55% en la riqueza de especies) fueron mucho mayores que las disminuciones de las especies terrestres (reducci�� on de 20% en 2008 y 24% en 2009). De manera similar, las abundancias de ranas en quebradas y arboreas �� fueron menores en el per�� ��odo combinado 2008���2009 que en 1999, mientras que las densidades de ranas en los cuadrantes de hojarasca no cambiaron en los a�� nos de muestreo. Estas disminuciones pueden estar asociadas con la infecci�� on de ranas con Bd. La prevalencia de B. dendrobatidis se correlacion�� o signi- ficativamente con la proporci�� on de especies que estuvieron ausentes en los muestreos de 2008 y 2009 a lo largo del gradiente altitudinal. Nuestros resultados sugieren que Bd pudo haber llegado al sitio entre 1999 y 2007, lo cual es consistente con la hipotesis �� de que este patogeno �� se est�� a dispersando en olas epid�� emicas a lo largo de las cordilleras Andinas. Nuestros resultados tambi�� en indican una rapida �� disminuci�� on de la riqueza de especies y abundancia de ranas en nuestra �� area de estudio, un parque nacional que contiene muchas especies de anfibios end�� emicas y tiene una gran riqueza de especies de anfibios. Palabras Clave: Andes tropicales, anfibios, especies amenazadas, gradiente altitudinal, extinci�� on, bosque montano, Neotropicos�� Introduction In addition to deforestation (Pineda & Halffter 2003 Gal- lant et al. 2007) and climate change (Raxworthy et al. 2008), the pathogen Batrachochytrium dendrobatidis (Bd) is associated with amphibian declines throughout the world (Berger et al. 1998 Briggs et al. 2005 Lips et al. 2006). These declines have been particularly severe in tropical mountains, where species have intrinsically higher probabilities of extinction because their ranges are restricted geographically (McDonald & Brown 1992). The hypothesis that Bd is an emergent disease is sup- ported by the fungus��� low genetic diversity (Morehouse et al. 2003), poor correlation between fungal genotypes and geography (Morgan et al. 2007), and epidemic level of infection and dramatic effect on na�� ��ve amphibian popula- tions (Berger et al. 1998 Vredenburg et al. 2010). B. den- drobatidis may have spread along the Andean cordilleras in three epidemic waves from two sites where it was introduced in the late 1970s or early 1980s, one in south- western Ecuador and the other in the Venezuelan Andes (Lips et al. 2008). One wave spread south and west of Venezuela, one spread north from Ecuador, and the third spread south from Ecuador. Lips et al. (2008) believe the systematic spread of Bd through areas with suitable cli- mates, geography, and host populations is analogous to an epidemic wave, in which a virulent pathogen spreads through na�� ��ve host populations. The rate of movement of the wave toward the Peruvian Andes was between 37 and 202 km/year. If Bd is spreading in an epidemic wave and there are no other introduction points of Bd in the Andes, Bd should have already reached southern Peru or will reach it by 2025. Chytridiomycosis in Peru was first recorded in 1999 in a population of Atelopus patazensis (Venegas et al. 2008) approximately 600 km south of the presumed introduction point in Ecuador (Lips et al. 2008). Seimon et al. (2007) detected Bd in two species of high-elevation frogs in southern Peru in 2002 and linked the appearance of this pathogen to de- clines in abundance. Therefore, we know that Bd has been affecting montane frogs in Peru since at least 1999. Moreover, Ron (2005) found the eastern slopes of the Peruvian Andes fell within the predicted distribution of the fundamental niche of Bd. We sought to examine whether amphibian species richness and abundance changed from 1999 to 2009 in a large national park in the Tropical Andes in the context of previous declines of Neotropical amphibian faunas. In addition, we considered whether Bd is spreading in the central Andes in epidemic waves. We compared our results with those of other studies of frogs conducted in Neotropical mountains. In particular, we examined similarities in groups of species, land-cover associations, and reproductive modes among species that declined at other sites. Because previous work suggests that epi- demic waves of chytridiomycosis resulted in major de- clines in frogs in northern South America, we assessed the potential influence of chytridiomycosis on amphib- ian declines in our study area. We hypothesized that the arrival of Bd in southern Peru and Bd infection of frogs is associated with declines in abundance and extirpations during our study period (1999���2009). Our approach al- lowed us to evaluate whether B. dendrobatidis may be driving declines of amphibian species richness and abun- dance in a protected area with minimal anthropogenic disturbance. Methods Study Sites The study sites were on the eastern slopes of the Cordillera de Paucartambo, Cusco, in the drainage basin Conservation Biology Volume **, No. **, 2010