In Florida's Lake Apopka, size does matter. Yet it took two years for
University of Florida zoologist Lou Guillette to believe his own
research findings. His data showed disturbing trends in the male alligator
population of this lake, located just outside of Orlando. The most striking
finding was the alligators' small penis size: 25% smaller than in normal males.
Furthermore, these males had testosterone levels as low as a typical
female's--a serious threat to their fertility. How had these "gender-bending"
defects occurred? Could manmade chemicals in the waters of Lake Apopka be
responsible? Concerned about the reproductive health of both wildlife and
humans, scientists everywhere began taking notice.
Catching alligators is no small feat. Alligators are nocturnal, and must be
studied at night. To find his alligators, Guillette takes to Lake Apopka in an
airboat and scans the darkened water with a high-powered flashlight. An
alligator's eyes reflect back the light, glowing red in the darkness. While
the airboat slowly approaches the animal, one of Guillette's intrepid graduate
students reaches out to grab it behind the head and hoist it onboard. Larger
animals are pulled alongside the boat with a noose. The team then takes blood
samples from each alligator and a variety of body measurements, including
Guillette uses phallus size as an indicator of proper hormone signaling. His
early research showed that alligators at Lake Apopka have abnormal levels of
the sex hormones estrogen and testosterone. What's more, he suspected that
contaminants in this pesticide-ridden lake might be blocking the male
alligators' response to their own testosterone. Guillette knew that penis
growth, whether in an alligator or a human, is dependent on testosterone--and
for normal alligators more testosterone means more growth. If chemicals were
blocking the effects of testosterone in these males, Guillette reasoned, he
should see it very clearly: Apopka's males would have shorter penises. Not
only that, but there would be no simple relationship between penis size and the
amount of testosterone in an alligator's system. Guillette tested this new
theory in the field.
What Guillette found in 1994-1995 was a 25% reduction in phallus size in both
juvenile and adult males from Lake Apopka. These animals had very low levels
of testosterone when compared to alligators from a healthy lake, Lake Woodruff.
This most likely contributed to their reduced penis size. But more
importantly, a Lake Apopka alligator's penis size did not faithfully reflect
the amount of testosterone in its blood. Something was preventing that
testosterone from having the intended effect.
By contrast, the alligators of Lake Woodruff developed normally. For them,
more testosterone meant larger phallus size. Lake Woodruff is located in a
national wildlife refuge on the St. Johns River, about 50 miles north of
Orlando, and is similar to Apopka in climate and food availability. In fact,
it is similar in all aspects save one: it has no history of pollution. And
significantly, Guillette found that alligator penises were shortest in that
part of Lake Apopka near the former Tower Chemical Company.
Guillette wondered if pollution could be causing the strange defects he found
at Lake Apopka. In 1980, Lake Apopka had been the site of a severe chemical
spill that left it one of Florida's most polluted lakes. A waste pond at the
Tower Chemical Company overflowed, spilling large amounts of the pesticides DDT
and dicofol into the lake. Soon afterward, 90% of Apopka's alligators
disappeared. Tissue samples from the remaining alligators showed high levels
of p,p'-DDE, a breakdown product of DDT, along with a host of other
contaminants. p,p'-DDE was the most common contaminant in the alligators'
eggs. In addition, Apopka suffered chemical runoff from agricultural areas
around the lake, and from a nearby sewage treatment plant. Could this be the
difference between Lake Apopka and Lake Woodruff? Could a spill that took
place over a decade earlier still be hurting the alligators of Lake Apopka?
Guillette still remembers when the pieces of this puzzle fell into place. It
happened when a colleague told Guillette what he had learned at a recent
meeting organized by Theo Colborn. Environmental contaminants, the colleague
said, could act like hormones. For example, p,p'-DDE, the major contaminant in
Lake Apopka, was known to block the action of testosterone. Suddenly, what
Guillette was seeing in Lake Apopka made sense; chemicals were disrupting
hormones in these animals.
While the waters of the lake were relatively clean, "gender-bending" pesticides
from the spill had moved into the food chain. Alligators were at the top of
that food chain, and accumulated contaminants like p,p'-DDE through the fish
that they ate. Females then deposited the chemicals in their eggs where they
could influence development of the embryos. It all made sense. The population
decline, the abnormal hormone levels, the strange structures Guillette had
found in the alligators' testes and ovaries...they were signs of scrambled
hormone signaling during development. Guillette was convinced that manmade
chemicals were the culprits.
For a scientist, however, correlation is not enough. Contaminants were present
in alligators with reduced penis size, but were they causing it? To prove that
contaminants could cause the problem, Guillette had to move his experiments
into the lab. If he could treat eggs in the laboratory with p,p'-DDE and show
the same abnormalities as in the wild, he would show that the chemical can
actually cause the problems. Guillette collected "clean" eggs from Lake
Woodruff for this experiment, and added contaminants to see what effect they
would have. Sure enough, a mixture of manmade chemicals could reproduce the
effects he saw in the wild. A mixture of the two most common contaminants in
Lake Apopka, DDD and DDE, did the trick. These chemicals caused depressed
testosterone, smaller penis size, and anatomical defects in male alligators
that would have otherwise hatched normally. In females, the chemicals caused
elevated estrogen levels. This was a clear indictment of manmade chemicals,
and Guillette's most provocative experiment to date.
When Guillette began studying Florida's alligators in 1985, he had no idea how
explosive his work would become. He had a simple goal: to survey the health of
the alligators. Alligator ranchers wanted to know how many eggs they could
collect and raise for hides without harming the population. Guillette and his
colleagues had identified lush Lake Apopka, Florida's fourth largest lake, as a
likely source. They soon discovered, however, that Apopka's alligator eggs
were in short supply. The alligator population was 90% smaller than it had
been a decade earlier, and the eggs there were three times as likely to die
before hatching as eggs from other lakes. Why were female alligators having
problems making good eggs?
To find out what was wrong, Guillette decided to raise some of these eggs in
the lab. In 1992, his research team collected eggs not only from this troubled
lake but also from Lake Woodruff where the alligator population was thriving.
The healthy eggs from Woodruff would be a "control" group, used for comparison.
That comparison proved informative. When baby alligators from each lake
finally hatched, the most obvious difference was in their viability: many of
the Lake Apopka hatchlings died within the first 10 days. But even more
significant differences emerged when Guillette began to measure hormone h old
Guillette found that Apopka's alligators had atypical hormone levels. Males
had the low testosterone levels of a female: over three times lower than in
normal males from Lake Woodruff. Apopka's females, for their part, had twice
the normal amount of estrogen. It appeared that the entire population had been
"feminized" during embryonic development. When Guillette looked closer, he
found abnormalities in the reproductive organs of these alligators as well.
Under a microscope, he could see that the males had poorly developed testes
that started to produce sperm unusually early in life. The females, too, had
unusual structures in their ovaries. Normally the ovaries contain many units
called follicles, each housing a single egg. In Lake Apopka females the
follicles housed up to three or four eggs, and those eggs had many nuclei
instead of just one. None of the Lake Woodruff alligators had these defects.
Convinced he must have done something wrong to get these results, Guillette
repeated his research the next year. The results were the same. It was then
that Guillette began to look at phallus size in these animals.
Recently, Guillette made another disturbing discovery. He found shorter
penises and abnormal hormone levels in alligators from other lakes, including
Lakes Okeechobee and Griffin. These are average lakes in the state of Florida,
not ones adjacent to a Superfund site like Lake Apopka. The finding has
scientists concerned. It suggests that background levels of contamination,
levels that humans are exposed to every day, could cause permanent changes in
developing young--at least in alligators. Guillette's biggest concern is that
these changes will reduce the ability of the alligator population to respond to
events like hurricanes and disease outbreaks. With their fertility on the
brink of disaster, an unwelcome challenge could still push them over the
Guillette LJ, et al. (1994). "Developmental Abnormalities of the Gonad and
Abnormal Sex Hormone Concentrations in Juvenile Alligators from Contaminated
and Control Lakes in Florida". Environmental Health Perspectives
Guillette LJ, et al. (1996). "Reduction in Penis Size and Plasma Testosterone
Concentrations in Juvenile Alligators Living in a Contaminated Environment".
General and Comparative Endocrinology 101:32-42.