Berkeley

Low levels of the most widely used herbicide in the United States have been found to disrupt the sexual development of frogs. The finding will heighten concerns about the persistence of endocrine-disrupting chemicals in the environment — and throws the spotlight on another potential factor involved in the global decline of amphibian populations.

In the United States, about 27,000 tonnes of atrazine are applied each year to fields used to grow crops such as maize, sorghum and sugar cane. It is also used in 80 other nations, making it one of the world's most important herbicides. But concerns about atrazine's potential ability to disrupt sex hormones, and the presence of residues in drinking water, have led it to be banned in Germany, France, Italy, Sweden, Norway and Switzerland.

Tyrone Hayes has fears for frogs.

Tyrone Hayes and his colleagues at the University of California, Berkeley, exposed tadpoles of the African clawed frog (Xenopus laevis) to water containing different levels of atrazine throughout their larval development. Levels as low as 0.1 parts per billion (p.p.b.) caused males to develop ovaries in addition to testes. And at concentrations above 1 p.p.b., male frogs' larynges — used to call for mates — failed to develop normally, Hayes reports in a paper published on 16 April (T. B. Hayes et al. Proc. Natl Acad. Sci. USA 99, 5476–5480; 2002).

In addition, when the researchers put adult males in water containing 25 p.p.b. of atrazine, their testosterone levels plummeted. And in preliminary, unpublished research, Hayes has found similar reproductive anomalies in wild leopard frogs (Rana pipiens) at six locations in the midwestern United States with high levels of atrazine.

“It is obviously affecting frogs,” says Hayes, who suspects that atrazine boosts production of the enzyme aromatase, which catalyses the conversion of testosterone into oestrogen. “We need to ask: what are the environmental costs of using atrazine?” he says.

Although previous studies have suggested that atrazine is an endocrine disrupter, these have mostly used much higher doses. Hayes's study is causing alarm because he has observed effects at concentrations that reflect those found in the environment. “Hayes's work is some of the best to show how a contaminant affects amphibian reproduction,” says Andrew Blaustein, who studies amphibians at Oregon State University in Corvallis.

“This is not a worst-case scenario where animals are exposed to mega-doses,” says Louis Guillette, a zoologist at the University of Florida in Gainesville. “These are concentrations we know wild amphibians are exposed to.” Indeed, atrazine is routinely found at 50 p.p.b. in water throughout the United States, experts say, and can rise to several parts per million in agricultural run-off.

Amphibians are highly sensitive to pollutants and are regarded as 'sentinel' species that can provide the first indications of damage to an ecosystem. Hayes's results come as the US Environmental Protection Agency (EPA) is re-evaluating the risks posed by atrazine — following a 1999 ruling on a lawsuit from the Natural Resources Defense Council and other environmental groups, requiring the agency to accelerate its efforts to reassess the environmental and health risks posed by a range of potential endocrine disrupters.

The EPA currently allows levels of atrazine to reach 3 p.p.b. in US drinking water. An EPA panel will hold a public meeting this week in Arlington, Virginia, on suggested residue levels of atrazine in food products.

Hayes has provided the EPA with a report on his unpublished fieldwork on frogs from Colorado to Wisconsin, but EPA officials declined to comment on this, or on Hayes's newly published paper. The agency aims to issue final reports on the risks posed by atrazine by August.

Atrazine is manufactured by Syngenta of Basel, Switzerland. Alan Hosmer, Syngenta's manager of ecological sciences in Greensboro, North Carolina, says that the firm is aware of some of Hayes's results. But the company failed to provide a detailed statement before Nature went to press. For three years, Hayes worked on contract research at Berkeley for Syngenta. But he severed relations with the firm last year, independently pursuing the studies that led to this week's paper.

Aside from their implications for the use of atrazine in the United States and elsewhere, Hayes's results add another element to the debate over why amphibian populations are declining across the world. Many factors are thought to be involved, including pathogens, pollution, competition with invading alien species, and habitat loss.

James Hanken, a herpetologist at Harvard University who chairs the international Declining Amphibian Populations Task Force, describes Hayes's results as “compelling”. But he notes that some of the most severe declines are in Central America, where atrazine is not thought to be widely used. Hanken argues that further studies are needed to determine what role atrazine and related chemicals are playing in amphibian declines across the globe.

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