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Amphibian mystery misread

A Correction to this article was published on 18 November 2009

A book blaming a fungus for the disappearance of amphibians from wild places wrongly downplays the role of environmental change, warn Alan Pounds and Karen Masters.

Extinction in Our Times: Global Amphibian Decline

  • James P. Collins &
  • Martha L. Crump
Oxford University Press: 2009. 304 pp. $29.95 9780195316940 | ISBN: 978-0-1953-1694-0

Across the globe, frogs, toads and salamanders are disappearing, even in protected habitats. In Extinction in Our Times, James Collins and Martha Crump try to reassure us that these vanishing creatures are not warning of large-scale environmental deterioration like canaries in a coal mine, but are simply “telling us that they themselves are in trouble”.

Amphibians such as this Tapichalaca tree frog are seen as bellwethers of environmental deterioration. Credit: FROGEVER.COM/L. A. COLOMA

The cause of amphibian declines in wild places, the authors assert, is often a single agent: the chytrid fungus Batrachochytrium dendrobatidis, which can produce a fatal skin disease in these animals. According to this view, the mass die-offs result from movement of the fungus between continents and across landscapes. However, this 'lone killer' hypothesis wrongly downplays the role of environmental change.

Collins and Crump see evidence for a lone-killer chytrid in reports that a wave of amphibian extinction spread with the fungus from northwest to southeast across Central America, beginning in the early 1980s. But this wave is still being evaluated. Federico Bolaños at the University of Costa Rica in San Pedro and his co-workers propose that it stems from biased sampling and from a failure to take into account all of the region's amphibian die-offs. Moreover, this pattern does not rule out the importance of environmental change in these declines. Studies of such losses must test hypotheses that consider multiple factors.

The authors recognize the interplay of factors, but treat this as a complication that obscures a simple reality. If the chytrid plays a part in a die-off, they reason, then other forces are not needed. This is like attributing a car crash to excessive speed and deciding that other contributing issues, such as alcohol consumption, need not be considered. Such a deterministic view of causation, blind to probabilistic influences, has no place in ecology. Nor is the simplest explanation necessarily the best. Collins and Crump invoke Occam's 'law of parsimony', but were Occam here today, he might quiz them about their assumptions.

For one, is the chytrid fungus really deadly? The resulting disease is sometimes lethal but often it is not, for reasons that go beyond genetics and history — environment matters in disease outcomes. Laboratory studies can be misleading: often they put amphibians under stress or erase the microclimatic heterogeneity that helps the animals to fend off disease. Such experiments can also exclude microbes that might otherwise keep the chytrid in check. Add to the picture how little we know about this fungus in the wild, especially outside its amphibian hosts, and the assumption that it is inherently lethal to many species becomes indefensible.

Amphibians are telling us one thing: Earth's life-support system is in trouble.

The chytrid's impact may instead depend on environmental changes. Collins and Crump's selection of published work and quoted opinions downplays such links. Nevertheless, studies show that increasingly extreme climate and weather, together with land-use change, pollution, ultraviolet (UV) radiation and species invasions, are degrading amphibian health in many regions. These factors can interact and their effects may cross the boundaries of protected areas. Associations between climatic changes and reduced amphibian survival have been found in western and eastern North America, Central and South America, Australia, Spain, Italy and England.

Evidence showing that amphibians have undergone climatic stress before chytrid outbreaks have taken place challenges the idea of a lone-killer fungus, yet Collins and Crump fail to acknowledge this. Instead, they argue that such evidence casts doubt on the largely untested 'chytrid-thermal-optimum' hypothesis, which proposes that microhabitat temperatures in many places are shifting towards the chytrid's optimum, thereby favouring this pathogen's growth and hindering amphibian defences. However, the climatic-stress hypothesis is compatible with this model. And contrary to the authors' claims, neither hypothesis assumes that the fungus is native to regions that are experiencing die-offs. Climate may influence a disease regardless of the pathogen's place of origin, and the presence of exotic microbes makes global warming an even greater threat.

The authors' narrow thinking biases their 'road map' for future research on amphibian declines. Consider UV radiation, which harms amphibians and interacts with pathogens, chemical pollution and climate in ways that scientists are only beginning to study. For example, global warming alters patterns of cloud cover, reducing UV exposure in some places and increasing it in others. By oversimplifying the issue, the authors suggest that UV radiation can be removed from the list of potential causes of amphibian die-offs.

Collins and Crump offer little comparison between amphibian declines and losses affecting other species. Organisms from lodgepole pines to African lions are dying en masse because of disease shifts that are linked to global warming and other environmental problems. For instance, in the wake of the European heatwave of 2003, many millions of invertebrate sea creatures, including sponges, molluscs and corals, died along several thousand kilometres of the northwest Mediterranean coastline. After studying a soft coral known as the red gorgonian, marine biologists Marc Bally and Joaquim Garrabou of the University of the Mediterranean in Marseille, France, reported that the high temperatures favoured certain bacteria that ravaged the coral. In Italy, a team led by Ines Di Rosa at the University of Perugia and Daniele Canestrelli at the University of Tuscia in Viterbo proposes that the heatwave had similar consequences for some of Italy's amphibians.

By asking how long it will be before amphibians are safe from the chytrid fungus, Extinction in Our Times misses the bigger picture. The interacting changes threaten many life forms. Di Rosa, Canestrelli and their colleagues are studying how climate change and pathogen movement may conspire to cause amphibian die-offs. In Costa Rica, where such losses have accompanied climate-related changes in populations of birds, reptiles, mammals, insects and plants, we are studying orchids that have recently begun to die in the cloud forest. Amphibians belong to a chorus of canaries telling us one thing: Earth's life-support system is in trouble.

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Pounds, J., Masters, K. Amphibian mystery misread. Nature 462, 38–39 (2009). https://doi.org/10.1038/462038a

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