Mixed Messages

Chemicals in the environment are disrupting critical internal communication systems in fish and other animals.

By Mary Hoff

Illustrations by Ron Finger

magazine spread: illustration of fish and chemical notations

Leroy Folmar had good news and bad news for his colleagues at the Minnesota Department of Natural Resources.

A research physiologist with the U.S. Environmental Protection Agency in Gulf Breeze, Fla., Folmar had spent the fall of 1995 working with DNR river surveys project supervisor Jack Enblom and DNR pathology lab supervisor Joe Marcino to see how the Metropolitan Wastewater Treatment Plant in St. Paul might be affecting the internal chemistry of fish in the Mississippi River. He had just finished testing blood from carp caught downstream from the plant. He was looking for the presence of vitellogenin, a protein female fish produce as part of egg-making.

The good news was the female carp were making plenty of the stuff.

The bad news? So were the males.

"The males were expressing these female proteins," Folmar says. "Their hormone balance was skewed toward that of a female."

Although they were the first such fish found in Minnesota, today we know that those sexually disrupted carp are far from alone. Across the state and around the world, scientists are accumulating evidence that homes, factories, and farms are releasing a variety of pollutants that share a troubling common trait: They interfere with the function of the endocrine system--the internal communication network that regulates numerous body functions, including development, growth, reproduction, metabolism, digestion, and reaction to stress.

Known collectively as endocrine disruptors, these substances and their precursors are found in municipal wastewater and medicine chests, paper-mill effluent and kitchen cupboards, farm fields and janitors' closets. They have been blamed for altering the reproductive systems of panthers, snapping turtles, and snails. Some scientists think they could be at least partly responsible for frog malformations observed in Minnesota in recent years. Researchers have linked them to a variety of ills, including thyroid enlargement in salmon, immune system malfunctions in seals, and behavioral aberrations in gulls. A 1997 roster compiled by the National Environmental Health Association listed 26 species, from sea urchins to humans, known to have been affected by endocrine disruptors.

How serious are these disruptions? Are they simply creating sideshow-type oddities? Or are they interfering with the ability of animals--including humans--to live and pass life on to the next generation? No one knows for sure. What we do know is that the chemicals that cause such disruptions appear to be remarkably diverse and ubiquitous. Human urine, plastics, cleaning supplies, toiletries, pesticides, PCBs, and more have all been implicated.

"Because endocrine systems are critical to normal reproduction and development," observes Gary Ankley, a toxicologist with the EPA's Mid-continent Ecology Division in Duluth, "the possibility that there may be a widespread distribution of chemicals in the environment that affect these systems is of significant concern."

In recent years scientists have come to recognize that many contaminants introduced into the environment can have a subtle but sobering impact--even in minute quantities. These chemicals make trouble not by outright poisoning, but by throwing a wrench into the relationship between chemical message carriers called hormones and their intended target.

Normally, hormones convey messages by binding to very specific structures on the surfaces of cells in a way that signals the cells to do or not to do certain things, such as make particular proteins. Endocrine disruptors appear to sabotage this process in several ways. Some prevent hormones from binding with the recipient cell. Others mimic the hormone, fooling the cell into making a product that is inappropriate and can cause a cascade of deleterious effects. Yet others stimulate or block the production of hormones, or prevent them from being decommissioned when their job is done. Depending on factors such as dose, duration, and stage of life, endocrine disruptors can cause anything from transitory cellular confusion to life-altering developmental abnormalities. And--this is the scary part--they can do so at astoundingly minute concentrations.

Widespread attention was first drawn to endocrine disruption in the environment in 1962, when marine biologist Rachel Carson forged a link between pesticide use and reproductive failure in birds with her now-famous book Silent Spring. In the four decades since, scientists have gathered evidence of problems. Alligators with abnormal testes and ovaries, fish carrying traits of both sexes, female herring gulls that paired with each other instead of with males, mink whose ability to reproduce was compromised--study after study has added evidence of a tapestry of trouble whose common thread is the endocrine system. And research intensified in the 1990s, thanks in part to efforts by World Wildlife Fund zoologist Theo Colborn and colleagues--including publication of the book Our Stolen Future in 1996--to encourage scientists and others to document, understand, and deal with what they call "hormone havoc."

More Questions Than Answers

The discovery by Folmar and colleagues of endocrine-disrupted carp in the Mississippi River in 1995 was followed by a spate of other studies aimed at assessing the occurrence of endocrine disruptors and disruption. What endocrine disruptors are out there, and where are they found? What other fish are affected? What, if anything, does the disruption mean to their ability to thrive and reproduce? "There were more questions than answers, that's for sure," Enblom says.

In a follow-up to the carp research, Folmar found that walleyes too appeared to be affected by the metro wastewater treatment plant effluent.

"Nobody blinked at the carp data, but when we found vitellogenin in male walleye, it was on the front page of the Star Tribune," he says.

Researchers from other federal agencies also checked out Minnesota waterways. In 1997 and 1998, U.S. Geological Survey scientist Larry Barber analyzed the metro plant's effluent and found alkylphenols, endocrine disruptors that are breakdown products of chemicals widely used in cleaning and personal care. Clifford Rice, a research chemist with the U.S. Department of Agriculture, found alkylphenols in walleyes caught downstream from the plant.

Two years ago University of Minnesota researchers led by Ira Adelman, Peter Sorensen, and Deborah Swackhamer searched for potential indicators of endocrine disruption in male walleyes taken near the metro plant.

They found not only high levels of vitellogenin, but also decreased gonad size. In a related lab study, Sorensen discovered that the effluent could induce vitellogenin production, reduce sperm count, and cause behavioral changes in goldfish.

In Lake Pepin, a team of USGS scientists led by fishery biologist Christopher Schmitt found male smallmouth bass with immature eggs in their testes. And last year Swackhamer reported that effluent from the Western Lake Superior Sanitary District treatment plant, which discharges to the Duluth-Superior harbor, induced vitellogenin production in fathead minnows in the laboratory.

So far, most research has focused on wastewater treatment plant effluent. But the problem appears to go beyond that. In 1999, led by USGS aquatic biologist Kathy Lee, researchers from the USGS, Minnesota Pollution Control Agency, and DNR looked for signs of endocrine disruption in male and female carp taken from 22 sites in 15 streams scattered across central and southern Minnesota.

They collected some carp from below wastewater treatment plants. Others they caught above dams that separated the fish from major sources of wastewater effluent. Fish from most sites showed potential signs of endocrine disruption--if not in vitellogenin, then in abnormal ovaries, testes, or sex hormone levels. Strangest of all, where male carp were collected above and below a wastewater treatment plant--with a dam in between--fish upstream tended to have higher vitellogenin levels. This finding led researchers to speculate that agricultural chemicals as well as substances contributed by wastewater treatment plants could be involved.

So What?

Even as scientists seek to solve the what, where, when, and how of endocrine disruption, they are also pursuing the answer to this compelling question: So what?

Probably the biggest concern in wild animals is related to effects endocrine disruption might have on their ability to reproduce. A 2000 book by the National Research Council concluded that environmental endocrine disruptors "probably have contributed to declines in some wildlife populations."

In a laboratory study, Sorensen and his associate Heiko Schoenfuss discovered that wastewater plant effluent induces changes in goldfish that are associated with decreases in sex drive and sexual behavior. The two are now conducting studies with minnows to see if such changes might have ramifications at the population level.

EPA's Ankley says there's good reason to believe that endocrine disruption could alter fish abundance. "We know there are chemicals in the environment that are affecting endocrine function in fish," he says. "It could be associated with a population-level effect. But we don't know what that link is quantitatively, or how widespread it is."

"I'm concerned that we're seeing vitellogenin in male fish in the wild even if we can't link it to a specific reproductive problem," Swackhamer says. "It just doesn't seem to be a good thing to have a male running around with a protein that's only supposed to be in females."

What about humans? Of course, people are not nearly as intimately associated with river water as are fish. Still, Colborn and others have cited numerous ways in which human reproduction and behavior seem to be changing in recent times (see Problems for People). Whether these are linked to the PCB-laden fish, plastics, and other endocrine disruptors that permeate our lives is yet to be determined.

"I think the jury is still out," says Hillary Carpenter, a toxicologist who has been following the issue for the Minnesota Department of Health. "We have sufficient information to indicate it is a problem in wildlife. We don't have that kind of information yet for human health."

Now What?

What can be done to reduce the threat of endocrine disruptors?

First, we can intensify efforts to remove known endocrine disruptors from the environment. Some such activity is already underway in the name of combating various chemicals' toxic, cancer-causing, or otherwise undesirable effects--for example, recent EPA-led efforts to remove PCB-contaminated sediments from the Hudson River. Other attempts at remediation--such as removing estrogens from municipal wastewater--may be more problematic.

"Activated carbon filtration would work, but it is expensive and the activated carbon would need to be properly disposed of," notes Swackhamer. "So one [would want] some indication that there is a risk before one required it of every treatment plant."

We can also reduce or eliminate further production of some culprits. This may be as complex as recent international efforts to reduce the use of PCBs, DDT, and other persistent organic pollutants, or as simple as switching detergent or hair-care products at home--if we can figure out which ones to eliminate.

The EPA is currently developing and carrying out a program for screening thousands of synthetic chemicals for endocrine disruptor activity.

"This is a Herculean task," says Eric A.E. Garber, a USDA Agricultural Research Service scientist who's been studying endocrine disruptors. "It's not just a matter of banning X, Y, and Z. The interplay of different compounds could make something that normally is not a concern a concern."

Connecting cause and effect is further complicated by the movement of chemicals through water, soil, and air, and by the presence of other factors such as water temperature and exposure to ultraviolet light that can cause changes that at first glance might seem to indicate endocrine disruption.

One thing is clear: We'll likely be hearing more about endocrine disruptors in the months and years to come. Minnesota has hundreds of wastewater treatment plants, each a potential source of endocrine-disrupting chemicals. Nobody knows how many other sources of endocrine disruptors might be out there. Researchers here have much yet to explore in terms of potential effects on species besides fish and frogs. They also have much to examine in terms of disruption of endocrine pathways controlled by the many hormones that regulate growth, metabolism, and other body functions besides reproduction.

"We're just at the tip of the iceberg now," Folmar says. "This is an area that's going to see a lot of attention."

A Few of the Suspects

Dozens of chemicals have been identified as having the ability, with varying degrees of potency, to interfere with the normal function of hormones. Among them:

  • Alkylphenols: Compounds that result from degradation of common cleaning and personal care products; mimic the female sex hormone estrogen.
  • Arsenic: A poisonous element; appears to alter the ability of glucocorticoid receptors, which regulate many body functions, to respond to hormones.
  • DDT: Pesticide banned in the United States but still sold and used in other parts of the world; disrupts calcium metabolism and functions regulated by estrogen.
  • Dioxins: Toxic compounds that are a byproduct of manufacturing; alter thyroid function and affect the ability of estrogen to do its job.
  • Estradiol: Hormone naturally produced and excreted by women; found in municipal sewage.
  • Ethynyl Estradiol: Hormone found in birth control pills and excreted in urine; ends up in wastewater treatment plant effluent.
  • PCBs: Pollutants that interfere with the activity of sex hormones and thyroid hormones.
  • Phthalates: Synthetic chemicals used in plastics; the most prevalent class in the environment. Mimic estrogen and block the action of male sex hormones. In laboratory rats, shown to reduce testosterone and produce abnormalities in the male reproductive system.
  • Phytoestrogens: Hormones found in soybeans, wheat, coffee, cherries, garlic, potatoes, carrots, apples, and hundreds of other plants; weak endocrine disruptors.

Problems for People

Exposure to endocrine-disrupting chemicals has "potentially serious consequences" for humans, according to the U.S. Environmental Protection Agency. Although connections have not yet been clearly drawn between cause and effect, some scientists speculate that recent trends in human health--including early puberty, reduced sperm count, and increased incidence of cancer of the breast, prostate, and testicles--are connected to the endocrine-disrupting molecules each of us encounters in the water we drink, the food we eat, the cosmetics we use, and the plastics that pervade our lives. Environmental endocrine disruptors are also being implicated in neurological and behavioral problems such as attention deficit hyperactivity disorder. Some of the evidence:

  • Children of women who ate rice oil laced with PCBs in 1968 and 1979 had low IQ, delayed development, and activity disorders. Boys had abnormally small penises.
  • Researchers found that children of women who ate a lot of Great Lakes fish had an unusually high incidence of behavioral and other nervous system problems.
  • A study of men exposed to the pesticide kepone at work showed they had unusually low sperm counts.
  • A recent report noted that adults exposed to large quantities of PCBs from Great Lakes fish had more learning and memory troubles than did other adults.

Mary Hoff

Mary Hoff is production coordinator for the Volunteer and a free-lance science writer. Ron Finger is an illustrator and graphic designer with Redpine, a studio in Baxter.