Riding the wave: reconciling the roles of disease and climate change in amphibian declines

Abstract

We review the evidence for the role of climate change in triggering disease outbreaks of chytridiomycosis, an emerging infectious disease of amphibians. Both climatic anomalies and disease-related extirpations are recent phenomena, and effects of both are especially noticeable at high elevations in tropical areas, making it difficult to determine whether they are operating separately or synergistically. We compiled reports of amphibian declines from Lower Central America and Andean South America to create maps and statistical models to test our hypothesis of spatiotemporal spread of the pathogen Batrachochytrium dendrobatidis (Bd), and to update the elevational patterns of decline in frogs belonging to the genus Atelopus. We evaluated claims of climate change influencing the spread of Bd by including error into estimates of the relationship between air temperature and last year observed. Available data support the hypothesis of multiple introductions of this invasive pathogen into South America and subsequent spread along the primary Andean cordilleras. Additional analyses found no evidence to support the hypothesis that climate change has been driving outbreaks of amphibian chytridiomycosis, as has been posited in the climate-linked epidemic hypothesis. Future studies should increase retrospective surveys of museum specimens from throughout the Andes and should study the landscape genetics of Bd to map fine-scale patterns of geographic spread to identify transmission routes and processes.

Figure 1. Graphical Representation of the Various Relationships Possible between DOD and LYO

Figure 2. Map of Central American Spreading Wave (Wave 1) with DOD Sites Indicated and Rate of Spread

DOD sites are indicated by open circles. Black bars indicate the hypothesized leading edge of the wave of Bd in the year indicated.

Figure 3. Map of South American Waves (Two Introductions; Waves 2, 3a, 3b, 4; See Text for Description of Waves), with DOD Sites Labeled and Rates of Spread Indicated between Black Bars

(1986) indicates A. pachydermus had an estimated DOD from 1986–1994, and we used the 1986 date. If we had used the 1994 date, the demarcation for spread would have moved north to the nearby 1987 locations. Earliest dates are in larger font and marked with an asterisk.

Figure 4. Evidence for Spatiotemporal Spread of Chytridiomycosis in Five Waves in Central and South America

The relationship between time since the earliest DOD within a wave and distance of spread of Bd was significant for (A) Wave 1 (p = 0.0067; β = 21.17; R ² = 0.97), (C) Wave 3a (p = 0.00153; β = 43.32; R ² = 0.47), (D) Wave 3b (p = 0.0050; β = 56.57; R ² = 0.40), and for (E) Wave 4 (p = 0.0279; β = 61.95; R ² = 0.49), but the relationship for (B) Wave 2 was not supported (p = 0.32).

Figure 5. The Strength of the Relationship between AT and LYO Decreased as Error Was Added Systematically to LYO

Plotted are the mean correlation coefficients (± 95% CI) for the relationship between AT and LYO. Numbers above the points represent the number of simulated runs that found a relationship equal to or greater in magnitude than that found in [17]. (A) Error is added symmetrically around LYO from a normal distribution of mean zero and increasing standard deviation. (B) Error is added forward in time from a uniform distribution. (C) Error is added forward in time with respect to LYO and is sampled from a Poisson distribution. (D) Error is added forward in time from an exponential distribution.

Figure 6. The Relationship between Time since the Earliest DOD (a Proxy for the Introduction of Bd) and Distance of Spread of Bd Was Robust to the Addition of Sampling Error

(A) When adding error backward in time from a uniform distribution, the relationship in Wave 1 remained statistically significant when random error up to 16 y was applied, in (B) Wave 3a up to 20 (+) y, in (C) Wave 3b up to 18 y, and in (D) Wave 4 up to 20 (+) y was applied.

Figure 7. Percentage of Atelopus Species Declined or Extinct by Elevation in our Study Area

Bars show the number of species at each elevation category while gray depicts the number of species in decline and white depicts stable species. The percentage of species in decline is written on each bar. Total number of species included in the analysis was 51.