Biological Conservation 144 (2011) 2913–2921 Contents lists available at SciVerse ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Factors related to the distribution and prevalence of the fungal pathogen Batrachochytrium dendrobatidis in Rana cascadae and other amphibians in the Klamath Mountains ⇑ Jonah Piovia-Scott a,b, , Karen L. Pope c, Sharon P. Lawler a,d, Esther M. Cole e, Janet E. Foley b a Center for Population Biology, University of California – Davis, One Shields Avenue, Davis, CA 95616, USA b Department of Veterinary Medicine and Epidemiology, University of California – Davis, One Shields Avenue, Davis, CA 95616, USA c United States Forest Service, Pacific Southwest Research Station, 1700 Bayview Drive, Arcata, CA 95521, USA d Department of Entomology, University of California – Davis, One Shields Avenue, Davis, CA 95616, USA e Department of Environmental Science and Policy, University of California – Davis, One Shields Avenue, Davis, CA 95616, USA article info abstract Article history: The fungal pathogen Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis, has Received 5 May 2011 been associated with declines and extinctions of montane amphibians worldwide. To gain insight into Received in revised form 29 July 2011 factors affecting its distribution and prevalence we focus on the amphibian community of the Klamath Accepted 22 August 2011 Mountains in northwest California. The Cascades frog (Rana cascadae), one of the most common amphib- Available online 5 October 2011 ians in these mountains, experienced increased mortality as a result of Bd exposure in laboratory trials and has experienced recent, dramatic declines in other parts of California. We surveyed 112 sites in Keywords: the Klamaths, all of which supported R. cascadae between 1999 and 2002, for amphibians and Bd to Chytridiomycosis (1) determine the distribution of Bd, (2) evaluate changes in the distribution of R. cascadae, and (3) assess Taricha granulosa Anaxyrus boreas associations between potential biotic and abiotic drivers and Bd infection. Bd was widely distributed in Pseudacris regilla the Klamath Mountains – we detected the pathogen at 64% of sites. R. cascadae was found at 79% of sites, Generalized linear mixed model and was often infected with Bd. These results suggest that Bd has not caused dramatic declines in R. cascadae in the Klamaths in recent years. Subadult R. cascadae had a higher Bd prevalence than other R. cascadae life stages (subadults: 36%, adults: 25%, metamorphs: 4%, larvae: 1%), and while the probabil- ity of infection decreased over the season for adults, it did not for subadults, suggesting that subadults may be more vulnerable to chytridiomycosis than other R. cascadae life stages. Bd prevalence in R. cascadae was highest early in the season at high-elevation sites, which may indicate that populations inhabiting high elevation sites may have a greater risk of being affected by chytridiomycosis. Three other common amphibian species also tested positive for Bd: Pacific chorus frog (Pseudacris regilla), western toad (Anaxyrus boreas), and rough-skinned newt (Taricha granulosa). Ó 2011 Elsevier Ltd. All rights reserved. 1. Introduction northern California (Fellers et al., 2008). Laboratory experiments have shown that exposure to Bd increases mortality in juvenile Chytridiomycosis, the disease caused by the fungal pathogen R. cascadae (Garcia et al., 2006), and Bd was discovered in multiple Batrachochytrium dendrobatidis (Bd), has been associated with R. cascadae populations in California in 2006 (Pope et al., unpub- extinctions and declines in amphibians worldwide (Skerratt et al., lished data), suggesting that chytridiomycosis may be a causal agent 2007; Fisher et al., 2009; Kilpatrick et al., 2010). For example, in the observed declines. The purpose of this study was to examine outbreaks of chytridiomycosis have caused the extinction of the distribution of Bd and R. cascadae in California’s Klamath Moun- hundreds of populations of mountain yellow-legged frog tains and identify biotic and abiotic factors associated with Bd (Rana sierrae/muscosa) in California’s Sierra Nevada Mountains infection. (Briggs et al., 2005; Rachowicz et al., 2006; Vredenburg et al., Bd infects the keratinized tissue of amphibians, including the 2010). A closely-related species, the Cascades frog (Rana cascadae), mouthparts of larvae and the skin of post-metamorphic animals has experienced severe declines in nearby mountain ranges in (Berger et al., 1998, 2005). The effects of Bd on larvae tend to be min- or, although sublethal and lethal effects have been described (Parris ⇑ and Cornelius, 2004; Blaustein et al., 2005; Garner et al., 2009). For Corresponding author at: Center for Population Biology, University of post-metamorphic amphibians, there is a great deal of variation California – Davis, One Shields Avenue, Davis, CA 95616, USA. Tel.: +1 530 754 9740; fax: +1 530 754 4837. among species in the effects of Bd, with some species experiencing E-mail address: [email protected] (J. Piovia-Scott). 100% mortality within weeks of exposure and others experiencing 0006-3207/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2011.08.008 2914 J. Piovia-Scott et al. / Biological Conservation 144 (2011) 2913–2921 few negative effects of infection (Skerratt et al., 2007; Fisher et al., vere declines have occurred in the southern Cascades, and the 2009; Kilpatrick et al., 2010). Environmental variables can also play few remaining populations consist of relatively small numbers an important role in the outcome of Bd infection. For example, labo- of frogs (Fellers et al., 2008). In contrast, there were still hundreds ratory experiments have demonstrated that elevated temperatures of R. cascadae populations found in the Klamath Mountains in can ameliorate the effects of Bd on infected individuals and help surveys conducted 1999–2002 (Welsh et al., 2006; Welsh and them clear infections (Retallick and Miera, 2007; Andre et al., Pope, unpublished data). The Klamath Mountains comprise a ser- 2008), and animals that behaviorally warm themselves can clear ies of ranges in northwestern California (Fig. 1). Elevations range infections (Richards-Zawacki, 2010). In addition, field studies have from 730 m to 2750 m, the dominant habitat types are mixed found lower prevalence of Bd at warmer sites (Woodhams and conifer and subalpine forests, and the climate is characterized Alford, 2005; Drew et al., 2006; Kriger et al., 2007; Walker et al., by moderately cold winters with heavy snowfall, and warm sum- 2010). Elevation has also been linked to outbreaks of chytridiomyco- mers with limited rainfall. The amphibian fauna of the Klamath sis. Many of the most dramatic amphibian die-offs have been Mountains includes five lentic-breeders (Cascades frog: R. casca- observed in montane areas (Fisher et al., 2009), and elevation is cor- dae, Pacific chorus frog: P. regilla [the boundary between P. regilla related with Bd prevalence in field studies (Woodhams and Alford, and its congener, Pseudacris sierra, is in the vicinity of our study 2005; Muths et al., 2008; Pearl et al., 2009b; Adams et al., 2010, region but its location has not been precisely determined but see Knapp et al., in press). As elevational changes are associated (Recuero et al., 2006b,a), so there is some taxonomic uncertainty with variation in temperature regimes, it is likely that these patterns associated with this species designation], western toad: A. boreas, are at least in part explained by differences in temperature. Seasonal long-toed salamander: Ambystoma macrodactylum, rough-skinned patterns in Bd prevalence are also likely to be influenced by temper- newt: Taricha granulosa) and two lotic-breeders (coastal tailed ature changes, although seasonal changes in the abundance of sus- frog: Ascaphus truei, Pacific giant salamander: Dicamptodon tene- ceptible amphibian life stages may also be important (Pearl et al., brosus). While we sampled all amphibians encountered, surveys 2009b; Adams et al., 2010; Russell et al., 2010; Kinney et al., 2011). focused primarily on lentic waters, so few lotic-breeding amphib- In addition to environmental drivers, the impact of Bd on host ians were sampled. populations may be linked to the density of amphibian hosts and We sampled sites in the Klamath Mountains that were found to the diversity of the host community. Host-pathogen dynamics are support R. cascadae in previous, comprehensive surveys of 915 len- often strongly dependent on host density, with increases in density tic waters in the Klamath Mountains (Welsh et al., 2006; Welsh expected to lead to higher transmission rates and faster spread of and Pope, unpublished data) using a geographically-stratified ran- pathogens through populations (Anderson and May, 1981). Host dom design . We first divided the 436 sites in the Klamath Moun- diversity can influence the prevalence of a pathogen by changing tains found to support R. cascadae in the 1999–2002 surveys the density of host species, altering host behavior, and allowing (Welsh et al., 2006; Welsh and Pope, unpublished data) into six poorly reservoir-competent host species to dilute the force of infec- geographic units (Marble Mountains Wilderness, Russian Wilder- tion or strongly reservoir-competent hosts to increase it (Keesing ness, Trinity Alps Wilderness, Shasta-Trinity National Forest [out- et al., 2006, 2010). However, while amphibian populations often ex- side