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The enemy next door

A common tropical fungus that is lethal to amphibians may be native to the Atlantic Forest

Despite its continuous presence in the environment, the disease does not affect species equally: it infects 75% of Bokermannohyla luctuosa...

célio haddad / unespDespite its continuous presence in the environment, the disease does not affect species equally: it infects 75% of Bokermannohyla luctuosacélio haddad / unesp

A fungus that has decimated amphibian populations in several countries may have originated in Brazil—more specifically, in the Atlantic Forest. That is the conclusion of a post-doctoral research study conducted by American biologist David Rodriguez in the laboratory headed by Kelly Zamudio at Cornell University. The finding contradicts the earlier notion that the disease was introduced into Brazil by frogs imported for meat production (see Pesquisa FAPESP Issue No. 196). But it was no surprise to Célio Haddad, a Brazilian biologist at the São Paulo State University (Unesp) in Rio Claro, who collaborated on the study. “When I was an undergraduate in the early 1980s, I saw a lot of tadpoles with completely deformed mouths,” he said. “Since the animals didn’t die of the condition, I didn’t consider it a problem.”

At the time, he didn’t know that the damage observed in tadpole mouths was the result of an infection by the chytrid fungus Batrachochytrium dendrobatidis. Although there were reports of mass die-offs among amphibians in the Americas and Australia beginning in the 1970s, particularly in higher-altitude regions, the culprit was not identified until the late 1990s.

In an effort to learn where on the planet the disease had first emerged, the Cornell/Unesp group examined 2,799 toads, frogs and tree frogs from 13 different families that had been collected between 1894 and 2010 in southern and southeastern Brazil. By swabbing certain areas of the body of each of the specimens stored in Brazilian museums and conducting genetic analysis at Cornell, the group found genetic material from the fungus in every family, according to a February 2014 article published in Molecular Ecology. The fungus had even infected the sample from 1894—the oldest on record so far. This finding means, of course, that we still do not know how long the disease has existed in the Atlantic Forest; we only know that 120 years ago it had already spread. The earlier records had been found in Africa in the 1930s, in addition to a suspected but unconfirmed specimen in Japan in 1902. Examining skin samples under a microscope in an earlier study, Haddad’s group had also detected the fungus in animals collected in Brazil in the 1960s.

In addition to confirming that the chytrid fungus has existed for a long time throughout the sampled region and across a wide diversity of species, the study also corroborates another of Haddad’s long-time suspicions: that there were no infestation peaks during that period that would be indicative of an epidemic. It appears that the disease—which is so lethal in other countries that it raises panic among experts at the prospect of forests full of dead animals—virtually never kills Brazilian amphibians. “Many of the infected animals we captured were reproducing, which means they were healthy,” explains the biologist, who is a leading expert in Brazilian frogs.


... and is absent in Hypsiboas polytaenius

célio haddad / unesp… and is absent in Hypsiboas polytaeniuscélio haddad / unesp

During a sabbatical at Cornell in 2013, Haddad discussed the findings with Rodriguez and, drawing on his own experience, confirmed what his younger colleague saw in the genetic data: B. dendrobatidis is part of the Atlantic Forest ecosystem. The prevalence of the fungus has remained constant since 1894, affecting about 20% of toads, frogs and tree frogs in southern and southeastern Brazil and following an endemic disease pattern. The study also identified two strains of the fungus, which can apparently form hybrids. One of them is typically Brazilian and less aggressive. The other is the more virulent form that has spread throughout several regions of the world.

The evidence presented by Rodriguez suggests that the chytrid fungus is native to the Atlantic Forest, and is not an invasive species that was introduced by the bullfrog trade in order to supply breeders who produce meat, beginning in the 1930s. On the contrary, it may have reached other countries through the exportation of such frogs and other amphibians. But no definitive conclusion can be reached as of yet. “The movement may have occurred in both directions,” Haddad points out. It is also possible that the global lineage arrived in Brazil before the late 19th century, but without causing much mortality because the Atlantic Forest frogs had already been “vaccinated” through contact with the less virulent Brazilian version, the biologist conjectures.

According to a comment by Karen Lips of the University of Maryland in the same edition of Molecular Ecology, the findings presented by the Cornell/Unesp group are changing our way of thinking about the origin, evolution and dissemination of the chytrid fungus throughout the world. Her opinion counts: Lips was one of the first researchers to study populations decimated by the fungus, and at a conference some 15 years ago, she expressed doubts about Haddad’s story that the disease did not cause serious harm here and was not even listed among the problems faced by frogs and related amphibians native to Brazil. In her opinion, the new knowledge also means that controlling the global trade in amphibians is not the best way to contain the disease. Indeed, it appears to have traveled around the world on its own, before it received any help to move between continents.

Diversity of anuran amphibians in the Atlantic Forest: origin, maintenance, and conservation (nº 2012/17220-0); Grant mechanism Post-doctoral research grant abroad – Regular; Principal investigator Célio Haddad (Unesp Rio Claro); Investment R$59,204.10 (FAPESP).

Scientific article
RODRIGUEZ, D. et al. Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Molecular Ecology, V. 23, No. 4, p. 774-87. Feb. 2014.