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Popular
weed killer demasculinizes frogs, disrupts their sexual development,
UC Berkeley study shows
04
April 2002
By Robert Sanders,
Media Relations
Berkeley – The
nation's top-selling weed killer, atrazine, disrupts the sexual development
of frogs at concentrations 30 times lower than levels allowed by the
Environmental Protection Agency (EPA), raising concerns about heavy use
of the herbicide on corn, soybeans and other crops in the Midwest and
around the world.
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An
African clawed frog, Xenopus laevis
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A restricted
herbicide, atrazine is used primarily on crops, not around the home,
and can be purchased and applied only by certified applicators.
In an article
in the April 16 issue of Proceedings of the National Academy of Sciences,
University of California, Berkeley, developmental endocrinologist Tyrone
B. Hayes, associate professor of integrative biology, and his colleagues
report that atrazine at levels often found in the environment demasculinizes
tadpoles and turns them into hermaphrodites - creatures with both male
and female sexual characteristics. The herbicide also lowers levels of
the male hormone testosterone in sexually mature male frogs by a factor
of 10, to levels lower than those in normal female frogs.
As Hayes
later discovered, many atrazine-contaminated ponds in the Midwest contain
native leopard frogs with the same abnormalities.
"Atrazine-exposed
frogs don't have normal reproductive systems," he said. "The males have
ovaries in their testes and much smaller vocal organs," which are essential
in calling potential mates.
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Abnormal
gonads in a male Xenopus frog, the result of exposure to the
herbicide atrazine. The frog has become a hermaphrodite, that is,
it has both male (testes) and female (ovaries) sex organs. Credit:
Tyrone Hayes/UC Berkeley, courtesy PNAS
High-resolution
image available for download.
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It is unclear
whether these abnormalities lead to reduced fertility. Hayes now is trying
to determine how the abnormalities affect the frogs' ability to produce
offspring.
"The use
of atrazine in the environment is basically an uncontrolled experiment
- there seems to be no atrazine-free environment," Hayes said. "Because
it is so widespread, aquatic environments are at risk."
Because
the herbicide has been in use for 40 years in some 80 countries, its
effect on sexual development in male frogs could be one of many factors
in the global decline of amphibians, he added.
The findings
come at a time when the EPA is re-evaluating allowable levels of atrazine
in drinking water, which stand today at 3 parts per billion (ppb), and
has drafted new criteria for the protection of aquatic life, limiting
four-day average exposures to 12 ppb. Hayes found hermaphroditism in
frogs at levels as low as 0.1 ppb. Even with today's limits, levels of
40 ppb atrazine have been measured in rain and spring water in parts
of the Midwest, while atrazine in agricultural runoff can be present
at several parts per million.
The herbicide
also contaminates drinking water supplies in many communities in the
Midwest, leading some environmental groups to voice concern about its
effect on children, infants and the fetus. France, Germany, Italy, Sweden
and Norway are among countries that have banned the use of atrazine.
"This is
very important and elegant work," said Theo Colborn, PhD, a senior scientist
at the World Wildlife Fund and an internationally recognized expert on
endocrine disrupting chemicals. "Tyrone's work demonstrates the need
to do research on the safety of chemicals in the field where the animals
live and at the levels to which they are exposed. The changes he found
in the gonads were not discovered with the traditional high-dose atrazine
experiments used in the past. In addition, microscopic examination of
the internal organs of the frogs is required to detect the hidden effects
from low-dose exposure."
To date,
atrazine's effects on mammals and amphibians have been tested only at
large doses, not at doses commonly found in the environment.
In their
journal article, Hayes and his colleagues write, "The effective doses
in the current study ... demonstrate the sensitivity of amphibians relative
to other taxa, validate the use of amphibians as sensitive environmental
monitors/sentinels, and raise real concern for amphibians in the wild."
Hayes doubts
that atrazine has such severe effects on humans, because the herbicide
does not accumulate in tissue and humans don't spend their lives in water
like frogs do. Nevertheless, the effects of atrazine on frogs could be
a sign that the herbicide is subtly affecting human sex hormones, too,
interfering with androgens, such as testosterone, that control male sex
characteristics.
Some studies
in cell culture point to a possible biochemical explanation for the observed
effects on amphibian sex organs. John P. Giesy, a professor of zoology
at Michigan State University in East Lansing, and his colleagues found
last year that, at large doses, atrazine ups production of the enzyme
aromatase, which converts androgen hormones to estrogen hormones. Extrapolating
these results from mammalian cells to amphibians, Hayes argues that atrazine
could feminize male frogs by promoting the conversion of male hormones
to female hormones. The lowered androgens would interfere with voice
box development, while increased estrogens would promote ovaries within
the testes.
More than
60 million pounds of the herbicide were applied last year in the United
States alone. Manufacturer Syngenta estimates that farmers use the herbicide
to control weeds on about two-thirds of all U.S. corn and sorghum acreage.
On average, it improves corn yield by slightly more than four percent.
The compound is generally considered safe, however, because it quickly
decomposes in the environment and, being water soluble, is quickly excreted
from the body.
Aquatic
life, however, swim and breed in atrazine-contaminated field runoff.
Though previous studies showed deformities and abnormalities in adult
amphibians only at very high doses, no one had looked in detail at hormone
levels in frogs or at effects on tadpoles, the larval stage of frogs.
Prodded
by the EPA, Syngenta approached Hayes, an expert on amphibian hormones,
to find out if atrazine disrupts sex hormones in amphibians. He has developed
several very sensitive assays to detect chemicals that affect hormones,
including a test for estrogen-like chemicals that might induce human
breast cancer.
Though
Hayes initially received funds from Syngenta for the studies, all the
current published studies were conducted independent of Syngenta.
For his
laboratory tests, he used the African clawed frog, Xenopus laevis,
a popular research subject that, like many frogs, is very sensitive to
hormones that mimic the effect of their own sex hormones. If raised in
a pond with estrogen, for example, all Xenopus tadpoles turn into females.
In the presence of androgens, frogs grow larger voice boxes, or larynges.
In laboratory
experiments at various concentrations of atrazine, using two separate
populations of frogs raised in three separate tanks - experiments replicated
51 times - they found atrazine to affect the sexual development of frogs
at concentrations of 0.1 ppb and higher. That is 30 times lower than
the allowable limit of 3 ppb in drinking water and 120 times lower than
the proposed chronic exposure limit for aquatic life, 12 ppb.
At these
concentrations, as many as 16 percent of the animals had more than the
normal numbers of gonads - including one animal with six testes - or
had both male and female organs (testes and ovaries). No control animal
had such abnormalities.
Also, while
normal males at metamorphosis have larger vocal organs than females,
the organs of more than 80 percent of males exposed to 1 ppb or more
of atrazine were smaller than average. Sexually mature males showed a
10-fold decrease in testosterone levels, bringing them below levels found
in normal females. This suggests that atrazine acts by disrupting the
synthesis of sex hormones, which could also explain the smaller larynges
and abnormal gonads.
"... the
current data raise new concerns for amphibians with regard to atrazine,"
the researchers wrote in their paper. "If such effects occur in the wild,
exposed animals would suffer impaired reproductive function."
In fact,
Hayes and his colleagues subsequently conducted a reconnaissance of atrazine-contaminated
ponds in the Midwest to see if such reproductive abnormalities occur
in frogs in the wild. They turned up many native leopard frogs (Rana
pipiens) with similar problems, and are now testing captured animals
to determine whether these changes are due to atrazine.
"Atrazine
is obviously affecting frogs," Hayes said. "We have shown serious effects
on their sexual development. We need to ask the questions, 'What are
the environmental costs of using atrazine? What diversity have we lost?'"
Hayes conducted
the study with the help of recent PhD recipient Nigel Noriega, research
associate Aaron Vonk, and former or current undergraduate students Atif
Collins, Melissa Lee, Magdelena Mendoz and A. Ali Stuart, all of whom
are listed as coauthors of the paper. The studies were supported by the
National Science Foundation.
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