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Riding the Wave: Reconciling the Roles of Disease and Climate Change in Amphibian Declines
Lips KR, Diffendorfer J, Mendelson III JR, Sears MW PLoS Biology Vol. 6, No. 3, e72 doi:10.1371/journal.pbio.0060072

Forgetting Habitat Loss in Amphibian Extinctions – Missing the Forest for the Disease
David Bickford, Lee TM, Koh LP, Sodhi NS, Diesmos AC, Brook BW, CH Sekercioglu, Bradshaw CJA (04 April 2008)
Amphibian extinctions: Disease not the whole story
Camille Parmesan, Michael C Singer (28 March 2008)

Forgetting Habitat Loss in Amphibian Extinctions – Missing the Forest for the Disease

David Bickford

Assistant Professor

National University of Singapore

E-mail

Additional Authors: Lee TM, Koh LP, Sodhi NS, Diesmos AC, Brook BW, CH Sekercioglu, Bradshaw CJA

Competing Interests: None

Submitted Date: March 28, 2008

Published: April 04, 2008

The recent review by Lips et al. on climate change triggering chytrid fungus outbreaks in Neotropical amphibians is an excellent investigation. Despite their comprehensive analysis and conclusion that the link between climate change and disease is tenuous, the paper epitomizes a current trend in amphibian extinction research: ignoring the primary factor. Habitat loss is clearly the most important driver of amphibian extinction, compounded by accelerating rates of forest loss. While we commend the authors for a rigorous treatment of an interesting and important issue, we must ensure we do not miss the forest for the trees.
Recent amphibian research and publications has shifted to topics that attract funding and top-tier publications (e.g., Berger et al. 1998; Blaustein and Kiesecker 2002; Pounds et al. 2006). We do not contest that climate change and disease are important drivers of amphibian decline; however, we do take issue with lack of recognition that these stressors are of relatively lower priority compared to habitat loss.
Recent work has clearly shown that amphibian threat and decline risk are determined primarily by a species’ range size and affected by habitat loss and fragmentation (Cooper et al. 2008; Sodhi et al. 2008). While it is fascinating that evidence to support climate change driving amphibian chytridiomycosis outbreaks is scant, attention to this issue draws awareness away from the highest conservation priority. Global net forest loss is occurring at a rate of 7.3 million ha year-1 (FAO , 2005), an area greater than the range of 73 % of the combined 2583 amphibian species analyzed by Sodhi et al. (2008).
To emphasize our point, we examined prevalence of ‘habitat loss/degradation (human-induced)’ and ‘pathogens/parasites’ as major threat types among amphibians compiled by the Global Amphibian Assessment in the IUCN Red List database (www.iucnredlist.org). Of 5880 extant amphibians, 3404 (58 %) are threatened by habitat loss (55 % listed as Vulnerable, Endangered, Critically Endangered, and Data Deficient; hereafter ‘red-listed’), only 78 (1 %) are affected by diseases (79 % of which are ‘red-listed’), and 461 (8 %) are impacted both by habitat loss and disease (85 % of which are ‘red-listed’).
We strongly argue that the best use of finite conservation resources is to concentrate on habitat protection and the synergies between habitat degradation and other stressors such as disease and climate change. If we fail to target the most important drivers of extinction and decline, we risk losing many more amphibians than have already disappeared.

References
Berger L, Speare R, Daszak P, Green DE, Cunningham AA et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95(15): 9031-9036.
Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5(4): 597-608.
Cooper N, Bielby J, Thomas GH, Purvis A (2008) Macroecology and extinction risk correlates of frogs. Global Ecology and Biogeography 17(2): 211-221.
FAO (2005). State of the World's Forests. Rome: Food and Agricultural Organisation of the United Nations
Lips KR, Diffendorfer J, Mendelson JR, Sears MW (2008) Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biology 6(3): e72.
Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL et al. (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439(7073): 161-167.
Sodhi NS, Bickford D, Diesmos AC, Lee TM, Koh LP et al. (2008) Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS One 3(2): e1636. doi:10.1371/journal.pone.0001636

Amphibian extinctions: Disease not the whole story

Camille Parmesan

Associate Professor

Integrative Biology, University of Texas at Austin

E-mail

Additional Authors: Michael C Singer

Competing Interests: None

Submitted Date: March 26, 2008

Published: March 28, 2008

Amphibians have been mysteriously going extinct worldwide. Lips et al.1 claim to have bolstered evidence for disease as the culprit, and refuted evidence of a climate change link. We argue that Lips et al.’s analyses of invasive spread of the fungus Batrachochrytium dendrobatidis (Bd) are questionable and that their critique of climate explanations is seriously flawed.

In attempts to discredit climate change as a causal factor in Central American extinctions, Lips et al. reveal serious statistical ignorance. Pounds et al.2 found highly significant associations between the last year a species was observed (LYO) and high temperatures in the prior year. Lips et al. criticize use of LYO as a surrogate for extinction: amphibian censuses are sporadic and sampling intensity variable, resulting in noisy datasets. However, Lips et al.’s re-analyses, which attempted to simulate uncertainty by adding large levels of error to LYO data, is statistically inappropriate. Increasing data noise (adding additional error) will eventually cause loss of any statistical relationship in any dataset. Therefore, Lips et al.'s re-analysis shows nothing beyond a known statistical property of all datasets: as random noise increases, the ability to detect a true relationship decreases.

Error in LYO should make finding a relationship more difficult, but should not bias the outcome towards a particular conclusion. Thus, the fact that Pounds et al. found significant relationships between climate and LYO indicates that the relationship was so strong that it was robust to any errors in estimates of year of extinction. Might this conclusion have been affected by bias? A systematic trend for researchers to alter their sampling in response to the previous year’s weather would do the trick. However, we find this scenario- of temperature-dependent variation in censusing techniques/intensity with 1-year lag time- to be implausible.

In advancing their argument that climate-independent spread of Bd is the cause of extinctions, Lips et al. draw maps of dates of first observed population decline (DOD), interpreting these as times of first arrival of Bd. However, DOD is not an appropriate surrogate for Bd arrival because Bd occurs in populations that are not declining3 and amphibians have disappeared in the absence of Bd4. Lips et al. postulate that Bd spread in “waves from 4 oldest records of decline.” Within 4 of 5 waves, they find a significant positive regression between distance from the oldest declines and subsequent DODs, a pattern which they argued fits a spread of disease from each focal point. But each ‘wave’ was arbitrarily delineated by starting from the oldest DOD records. Observations inconsistent with a single ‘wave’ were reconciled by adding waves until a consistent pattern was achieved. While this may correctly represent events, this procedure weakens the impact of statistical significances.

In conclusion, the Pounds et al. study2 shows that patterns of amphibian extinctions (LYO) in space (elevation) are moderately consistent with climate change being the driver, and that amphibian extinctions (LYO) in time are strongly consistent with climate change being the driver (extinctions being high after hot or dry years)2,3. The Lips et al. study1 shows that spatiotemporal patterns of amphibian decline (DOD) are moderately consistent with disease spread (Bd) being the driver. These two hypotheses are both supported by multiple studies, are not mutually exclusive, and may in fact be interactive.

1. Lips KR, Diffendorfer J, Mendelson JR III, Sears MW (2008) PLoS Biol 6(3):e72. doi:10.1371/journal.pbio.0060072

2. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, et al. (2006) Nature 39: 161–167.

3. Retallick RWR, McCallum H, Speare R (2004) PLOS Biol 2:e351. doi:10.1371/journal.pbio.0020351

4. Pounds JA, Fogden MPL, Campbell JH (1999) Nature 398: 611–615.