Evaluating the links between climate, disease spread, and amphibian declines

Abstract

Human alteration of the environment has arguably propelled the Earth into its sixth mass extinction event and amphibians, the most threatened of all vertebrate taxa, are at the forefront. Many of the worldwide amphibian declines have been caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd), and two contrasting hypotheses have been proposed to explain these declines. Positive correlations between global warming and Bd-related declines sparked the chytrid-thermal-optimum hypothesis, which proposes that global warming increased cloud cover in warm years that drove the convergence of daytime and nighttime temperatures toward the thermal optimum for Bd growth. In contrast, the spatiotemporal-spread hypothesis states that Bd-related declines are caused by the introduction and spread of Bd, independent of climate change. We provide a rigorous test of these hypotheses by evaluating (i) whether cloud cover, temperature convergence, and predicted temperature-dependent Bd growth are significant positive predictors of amphibian extinctions in the genus Atelopus and (ii) whether spatial structure in the timing of these extinctions can be detected without making assumptions about the location, timing, or number of Bd emergences. We show that there is spatial structure to the timing of Atelopus spp. extinctions but that the cause of this structure remains equivocal, emphasizing the need for further molecular characterization of Bd. We also show that the reported positive multi-decade correlation between Atelopus spp. extinctions and mean tropical air temperature in the previous year is indeed robust, but the evidence that it is causal is weak because numerous other variables, including regional banana and beer production, were better predictors of these extinctions. Finally, almost all of our findings were opposite to the predictions of the chytrid-thermal-optimum hypothesis. Although climate change is likely to play an important role in worldwide amphibian declines, more convincing evidence is needed of a causal link.

Fig. 1.

Evaluation of the chytrid-thermal-optimum hypothesis. (A) Proportion of Atelopus species extinctions through time (closed circles), and the difference in the mean daily maximum and mean daily minimum temperatures in warmer months (open circles; March–October) for the region where Atelopus spp. inhabit. Also shown are the best-fitting third-order polynomial curves selected by using AIC (Table S2 and Table S3). The relationship between temperature difference and time was similar for cooler months (November–February) and, thus, is not displayed. Weighting the analyses by the number of extant species did not affect the statistical results or the model selection. Also shown is the less satisfactory linear fit through time (dashed lines), as suggested by Pounds et al. (4), for both Atelopus spp. extinctions and the difference in the mean daily maximum and mean daily minimum temperatures. (B) Relationship between temperature and exponential growth rate of Bd, per day, in culture based on the data of Piotrowski et al. (44) and Woodhams et al. (33), and the associated best-fitting third-order polynomial curves: y = −0.0001414x³ + 0.0047943x² − 0.0172752x − 0.0019076, R² = 0.9898; y = −0.0003107x³ + 0.0099077x² - 0.0176078x + 0.0000000, respectively). For the Woodhams et al. (33) data, we assumed that there was no chytrid growth at zero and 30°C. (C) Relationship between the proportion of Atelopus spp. extinctions and mean percent cloud cover in the previous year (open symbols, F_1,17 = 5.14, P = 0.037, R² = 0.232) and predicted mean Bd growth rate in the previous year (closed symbols, F_1,17 = 5.70, P = 0.029, R² = 0.251). (D) Relationship between the proportion of Atelopus species extinctions, and the difference between mean daily maximum and mean daily minimum temperatures in the previous year (F_1,17 = 0.020, P = 0.889, R² = 0.001). Results were consistent for both warmer and cooler months. (See Methods and Materials for details.)

Fig. 2.

Bd growth, cloud cover, temperature convergence, and temperature, through time, for the region inhabited by Atelopus spp. (A) Predicted mean regional Bd growth rate through time, based on mean regional temperatures (open circles; F_1,28 = 10.80, P = 0.003, R² = 0.278) and mean regional daily minimum temperatures (closed circles; F_1,28 = 5.85, P = 0.022, R² = 0.173). (B) Predicted mean regional Bd growth rate through time, based on mean regional daily maximum temperatures (open circles, F_1,28 = 19.60, P < 0.001, R² = 0.412). (C) Mean air temperature (open circles; F_1,26 = 9.94, P = 0.004, R² = 0.276) and cloud cover through time (closed circles; F_1,26 = 6.79, P = 0.015, R² = 0.207; arcsine square root-transformed). (D) Mean Bd growth rate through time for four elevation categories. (E) Mean cloud cover through time for four elevation categories. (F) Nonlinear relationship for mean daily maximum temperature minus mean daily minimum temperature, through time, for four elevation categories. For all images, either best-fit lines or curves are provided. For D and E, we have provided the results for the relationship between time and the response for each elevation category (*, P < 0.05; **, P < 0.01; NS = P > 0.05).

Fig. 3.

Frequency distribution for the last year observed minus the year of decline data from Lips et al. (18), and normal (mean = 4.23, SD = 6.56), uniform (mean = 1.63), Poisson (lambda = 3.73), exponential (rate = 0.0237), Weibull (shape = 0.833, scale = 4.20), and negative binomial (size = 0.203, μ = 3.73) fits. All four of the distributions (normal, uniform, Poisson, and exponential) used by Lips et al. (12), and the Weibull, were significantly different from the observed distribution (P < 0.000003). The observed distribution was not significantly different from a negative binomial distribution (P = 0.700). There was a total of 44 species used in this analysis. For species with ranges of years for their year of decline, we used the mean of the range.