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"If you look at one of these frogs, it's probably a hermaphrodite - plus, it metamorphoses late, which means it is subject to its pool drying up before it can become a frog," said lead researcher Tyrone Hayes, professor of integrative biology at U.C. Berkeley, and a Pesticide Action Network associate. "It's also smaller, if it metamorphoses at all, which increases the likelihood it will be eaten and decreases its ability to eat. Plus, it's immuno-suppressed, and more prone to die from infection." The group observed that mixtures of pesticides that accumulate in ponds near farms increased frog stress hormone levels, creating holes in the thymus gland that likely causes the impaired immune response.
"It's not the pesticides alone or introduced predators or ultraviolet light or global warming that's causing this decline, but the interaction between these on an animal that is pretty sensitive to its environment," said Hayes.
In research conducted four years ago, Hayes showed that atrazine, the most common weed killer used on corn in the United States, disrupts the sexual development of frogs by producing more hermaphrodites, decreasing the size of their vocal organs (critical to mating success), and causing a tenfold drop in testosterone in mature male frogs.
In one of the studies published online in Environmental Health Perspectives, Hayes reported even stronger evidence that atrazine, a powerful endocrine disruptor, both chemically castrates male frogs by blocking the action of the male steroid androgen and by stimulating the production of the female hormone estrogen. He was able to produce identical hermaphroditic malformations in frogs by administering estrogen or blocking androgen at the proper time of development.
"One week of exposure at the critical time is all that's required to make these males look feminine, which probably interferes with mating," he said. While noting that some frogs seem to adapt to atrazine by delaying development, presumably so that the critical developmental period takes place when the herbicide is at its lowest, Hayes suspects that not all frogs would adapt quickly enough to survive. Plus, delayed maturation comes at the risk of having the pond turn into a puddle and dry up before the frog completely metamorphoses.
In the other study also published online in Environmental Health Perspectives, Hayes looked at the combined effect of various pesticides on the health of frogs. His research group again examined atrazine as well as three other herbicides, two fungicides and three insecticides used on Midwestern cornfields. All nine were found in the scientists' study area in Nebraska in pools of water beside cornfields early in the growing season, when spraying typically occurs. Levels ranged from 0.1 parts per billion (ppb) to 10 or more ppb.
Hayes and his colleagues analyzed four years of data indicating that while some of the pesticides, herbicides and fungicides used on corn fields may not by themselves have a noticeable impact on frogs, in combination they create significant effects. Among these are delayed maturation (the tadpoles take longer to metamorphose into frogs), retarded growth, and an increased susceptibility to meningitis caused by normally benign bacteria.
When pesticides were combined, they had a stronger effect. All nine compounds together at 0.1 ppb - one of the lower concentrations measured in the field - lengthened the time to metamorphosis by 15 days, or about 25 to 30 percent. The mixture also caused a frog mortality of 35 percent.
All nine compounds together also produced a startling effect: the longer a tadpole took to mature into a frog, the smaller it was. It's normally the other way around, Hayes said. Separately, six of the pesticides did not affect this correlation, but three disrupted frog metamorphosis to the degree that there was no relationship between time and size. "In humans, this is like saying, 'The longer you are pregnant, the smaller your baby will be,' which means the womb is no longer a nurturing environment," Hayes said.
"Estimating the ecological risk and the impact of pesticides on amphibians using studies that examine single pesticides at high concentrations only may lead to gross underestimations of the role of pesticides in amphibian declines," Hayes concluded.
Hayes' laboratory colleagues were UC Berkeley students Paola Case, Sarah Chui, Duc Chung, Cathryn Haefele, Kelly Haston, Melissa Lee, Vien Pheng Mai, Youssra Marjuoa, John Parker and Mable Tsui. Co-authors on the atrazine paper were former UC Berkeley students A. Ali Stuart, Atif Collins, Nigel Noriega, Aaron Vonk, Gwynne Johnston and Dzifa Kpodzo, and current students Magdalena Mendoza and Roger Liu.
The work was supported by the National Science Foundation, Henry H. Wheeler, the Park Water Co. and the Howard Hughes Biology Scholars' Program.
Hayes, Tyrone B., et al. 2006. " Characterization of atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen (estradiol 17Beta]): Support for the demasculinization /feminization hypothesis." Environmental Health Perspectives Online , published January 24th, 2006. http://www.ehponline.org/members/2006/8067/8067.pdf