Seasonal Variation in Population Abundance and Chytrid Infection in Stream-Dwelling Frogs of the Brazilian Atlantic Forest

Abstract

Enigmatic amphibian declines were first reported in southern and southeastern Brazil in the late 1980s and included several species of stream-dwelling anurans (families Hylodidae and Cycloramphidae). At that time, we were unaware of the amphibian-killing fungus Batrachochytrium dendrobatidis (Bd); therefore, pollution, habitat loss, fragmentation and unusual climatic events were hypothesized as primary causes of these declines. We now know that multiple lineages of Bd have infected amphibians of the Brazilian Atlantic forest for over a century, yet declines have not been associated specifically with Bd outbreaks. Because stream-dwelling anurans occupy an environmental hotspot ideal for disease transmission, we investigated temporal variation in population and infection dynamics of three stream-adapted species (Hylodes asper, H. phyllodes, and Cycloramphus boraceiensis) on the northern coast of São Paulo state, Brazil. We surveyed standardized transects along streams for four years, and show that fluctuations in the number of frogs correlate with specific climatic variables that also increase the likelihood of Bd infections. In addition, we found that Bd infection probability in C. boraceiensis, a nocturnal species, was significantly higher than in Hylodes spp., which are diurnal, suggesting that the nocturnal activity may either facilitate Bd zoospore transmission or increase susceptibility of hosts. Our findings indicate that, despite long-term persistence of Bd in Brazil, some hosts persist with seasonally variable infections, and thus future persistence in the face of climate change will depend on the relative effect of those changes on frog recruitment and pathogen proliferation.

Fig 1. Mean number of individuals, temperature and precipitation.

Four-year time series data of: (A) the mean number of individuals found in four stream transects, and (B) monthly minimum temperature (°C) and precipitation (mm) at Parque Estadual da Serra do Mar, Brazil. Shaded bars highlight Batrachochytrium dendrobatidis swab sampling. The first asterisk (dead or dying frog) for C. boraceiensis represents two individuals found within 3 days. Sampling began February 2007 and continued monthly through January 2011.

Fig 2. Seasonal decomposition of frog abundance, temperature and precipitation.

Seasonal decomposition of the time series data of: (A) the mean number of individuals found in four stream transects, and (B) monthly minimum temperature (°C) and precipitation (mm) at Parque Estadual da Serra do Mar, Brazil.

Fig 3. Frog abundance, temperature and precipitation.

Trends of the time series data of: (A) the mean number of individuals found in four stream transects, and (B) monthly minimum temperature (°C) and precipitation (mm) at Parque Estadual da Serra do Mar, Brazil.

Fig 4. Intensity of Bd infection.

Batrachochytrium dendrobatidis infection intensity of Cycloramphus boraceiensis (Cb), Hylodes asper (Ha) and Hylodes phyllodes (Hp) during winter and summer stream surveys at Parque Estadual da Serra do Mar, Brazil. The total number of individuals swabbed is shown in the bottom of each bar. We measured genomic equivalents (GEs) using qPCR, and report the proportion of individuals infected by each zoospore category: 0, 1–10, 11–100, 101–1000, and >1001 GEs.