Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease

Abstract

The role of global climate change in the decline of biodiversity and the emergence of infectious diseases remains controversial, and the effect of climatic variability, in particular, has largely been ignored. For instance, it was recently revealed that the proposed link between climate change and widespread amphibian declines, putatively caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), was tenuous because it was based on a temporally confounded correlation. Here we provide temporally unconfounded evidence that global El Niño climatic events drive widespread amphibian losses in genus Atelopus via increased regional temperature variability, which can reduce amphibian defenses against pathogens. Of 26 climate variables tested, only factors associated with temperature variability could account for the spatiotemporal patterns of declines thought to be associated with Bd. Climatic predictors of declines became significant only after controlling for a pattern consistent with epidemic spread (by temporally detrending the data). This presumed spread accounted for 59% of the temporal variation in amphibian losses, whereas El Niño accounted for 59% of the remaining variation. Hence, we could account for 83% of the variation in declines with these two variables alone. Given that global climate change seems to increase temperature variability, extreme climatic events, and the strength of Central Pacific El Niño episodes, climate change might exacerbate worldwide enigmatic declines of amphibians, presumably by increasing susceptibility to disease. These results suggest that changes to temperature variability associated with climate change might be as significant to biodiversity losses and disease emergence as changes to mean temperature.

Fig. 1.

Time series of annual proportion of Atelopus species that began to decline (YOD) and that were observed for the last time (LYO) fit with the GAM. Shown are the final fitted cubic spline functions (solid lines) and associated 95% confidence bands (dashed lines). The relationship between year and both YOD (A) and LYO (B) was significantly nonlinear (df = 3.997, coefficient = 0.019, P = 0.006, R² = 68.17; and df = 3.997, coefficient = 0.011, P = 0.020, R² = 58.34, respectively).

Fig. 2.

Time series of Niño 3.4, temperature anomalies, AVMD of anomalies, and detrended YOD and LYO. YOD and LYO represent the annual proportion of Atelopus species that began to decline and that were observed for the last time, respectively. Note the concordance of the peaks and valleys of each dataset. All time series were loess smoothed. Niño 3.4 and temperature anomalies are presented as monthly data, whereas AVMD, YOD, and LYO are presented as annual data. Thirty-six and 14 species remain extant at the end of the time series for the LYO and YOD datasets, respectively.

Fig. 3.

Results of a path analysis testing for relationships among Niño 3.4, AVMD, DTR, and detrended LYO the following year. Probability values, standardized coefficients, and scatter plots, respectively, are provided next to each path. The scatter plots are based on the residuals from the relationship between AVMD and DTR. The model χ² was 0.298 (df = 1, P = 0.585), indicating that the model was a good fit to the data.

Fig. 4.

Testing for concordance between the spatiotemporal patterns of Bd-related declines and AVMD and DTR. Relationship between AVMD (•) or DTR (○) and (A) annual temperature, (B) elevation, and (C) monthly temperature. Data points with different letters are significantly different from one another (P < 0.05) according to a Fisher least significant difference test. Capital letters correspond to DTR, and lowercase letters correspond to AVMD.