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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.
Tyrone
Hayes with Colorado river toad (Bufo alvarius). Peg Skorpinski photo.
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
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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.
Prof.
Hayes and recent graduate Gwynne Johnston measure the length of a frog. Peg
Skorpinski photo.
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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