Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian

Abstract

Briggs. 2017. Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian. Ecosphere 8(3):e01740. 10. 1002/ecs2.1740 Abstract. Freshwater biodiversity is imperiled across the globe, and multiple stressors such as habitat alteration, non-native species invasion, disease, and climate change can act in concert to threaten vulnerable taxa. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis, is one of the causative factors of severe amphibian declines. The foothill yellow-legged frog (Rana boylii) is a stream-breeding anuran endemic to California and Oregon (USA) that has declined precipitously in recent decades, yet there is little information on its susceptibility to Bd. In the fall of 2013, we observed dead and dying juvenile R. boylii in a San Francisco Bay Area watershed where annual amphibian breeding censuses have been conducted since 1997 in a free-flowing reach and since 2003 in an anthropogenically modified stream reach. High pathogen loads on R. boylii and histologic lesions observed on a dead R. boylii metamorph collected from the site were consistent with lethal chytridiomycosis. The outbreak coincided with extremely low stream flows in autumn that concentrated frogs in drying pools and the absence of high peak flows in winter that allowed non-native American bullfrogs (Rana catesbeiana) to expand their spatial distribution in the stream network. Following the outbreak, we surveyed R. boylii and sympatric anurans at the site for the next two years to determine Bd trends within the population. Using mixed-effects models, we found that bullfrog presence was a positive predictor of both Bd prevalence and Bd load in R. boylii. Prevalence was also influenced by sex and life stage: Adult males were more likely to be infected than either females or juveniles. Moreover, we found that stream flow volume was negatively associated with Bd load. These results indicate that disease, drought, and flow regulation may interact synergistically to impact amphibians in ways not previously recognized, informing stream flow management strategies for native aquatic taxa.

Rapid extirpation of a North American frog coincides with an increase in fungal pathogen prevalence: Historical analysis and implications for reintroduction

“…While some laboratory studies have suggested that bullfrogs may not always make suitable reservoir hosts for Bd (Eskew, Worth, Foley, & Todd, ; Gervasi et al., ), our observation that bullfrogs have the highest Bd prevalence and loads among species sampled in the field (Figure ), and previous work showing that bullfrog sympatry is an important predictor of Bd infection in R . boylii (Adams et al., ), supports the hypothesis that bullfrogs are a vector of Bd in California, including where R . boylii are extant.…”

“…Although the interviews and histological examinations presented here, combined with a field study (Adams et al., ), indicate that R . boylii populations in central and northern California have also been affected by Bd and flooding, differences in environmental context may have contributed to a different outcome.…”

“…boylii indicates that Bd prevalence and loads are highest in R. catesbeiana (American bullfrog) and H. regilla (Figure ). Both R. catesbeiana and H. regilla are considered to be vectors of Bd in California (Adams et al., ; Padgett‐Flohr & Hopkins, ; Reeder et al., ), and as an often‐tolerant Bd reservoir host, bullfrogs have been implicated in declines of amphibians in places throughout the world where they are not native, including California (Daszak et al., ; Jennings & Hayes, ; Miaud et al., ). H. regilla and R. catesbeiana may have provided sufficient reservoir hosts to allow for Bd persistence in the system, facilitating chytridiomycosis‐induced extinction of R .…”

“…boylii in central California, water temperature was not predictive of either Bd prevalence or load in R . boylii , although low stream flows were predictive (Adams et al., ). Therefore, it may be other aspects of climate beyond ambient temperatures (i.e., precipitation, alternation of extreme droughts and floods) that distinguish the southern part of R .…”

“…In 2013, a central California population of R . boylii experienced a chytridiomycosis‐induced mortality event (Adams et al., ), the first such record for this species in the wild.…”