By Andy Coghlan
NewScientist.com

Wednesday 01 September 2004

Hyperactive fish, stupid frogs, fearless mice and seagulls that fall over. It sounds like a weird animal circus, but this is no freak show. Animals around the world are increasingly behaving in bizarre ways, and the cause is environmental pollution.

The chemicals to blame are known as endocrine disruptors, and range from heavy metals such as lead to polychlorinated biphenyls (PCBs) and additives such as bisphenol A.

For decades, biologists have known that these chemicals can alter the behavior of wild animals. And in recent years it has become clear that pollutants can cause gender-bending effects by altering animals' physiology, particularly their sexual organs.

But now two major reviews have revealed that the chemicals are having a much greater impact on animal behavior than anyone suspected. Low concentrations of these pollutants are changing both the social and mating behaviors of a raft of species. This potentially poses a far greater threat to survival than, for example, falling sperm counts caused by higher chemical concentrations.

Snails and Quails
The two research teams have independently collected evidence revealing the effects on egrets and gulls, snails, quails, rats and macaques, minnows, mosquito fish, falcons and frogs. Behaviors altered include mating and parenting, nest building, learning, predator avoidance, foraging, activity levels and even balance.

In one study, for instance, male starlings exposed to dicrotophos insecticide decreased their singing, displaying, flying and foraging activities by 50%. And newts exposed to low levels of the pesticide endosulfan found it harder to sniff out the attractive pheromones of potential mates.

Researchers have also shown that increasing numbers of male western gulls hatched from eggs exposed to DDT attempt to mate with each other. In recent years, scientists have also found that lead affects the balance of gulls, while atrazine makes goldfish hyperactive and the chemical TCDD makes the play behavior in macaques rougher.

Despite this wealth of evidence, these effects have gone largely unnoticed by toxicologists, says Ethan Clotfelter of Amherst College in Massachusetts, lead author of one of the reviews, published in August 2004 in Animal Behavior (vol 68, p 465).

Missing a Trick
Not only are we failing to acknowledge the scale of the problem caused by endocrine disruptors, but toxicologists may be missing a trick: changes in animal behavior could be an early warning that certain chemicals are harmful. "You might see behavioral effects long before you see a population crash," Clotfelter says.

Dustin Penn and Sarah Zala of the Konrad Lorenz Institute of Comparative Ethology at the Austrian Academy of Sciences in Vienna agree. They have just published a second review of the effects of endocrine disruptors in the same journal (DOI: 10.1016/j.anbehav.2004.01.005). "The most important point is the incredible amount of evidence that this is a widespread problem," Penn says.

Both research groups say that biologists must wake up to the fact that endocrine disruptors might explain bizarre behavior in wild animals. And both reviews reveal that different concentrations of chemicals can have unexpected effects.

Male mice exposed to low doses of some pesticides increase their scent-marking behavior, for instance, but decrease it when exposed to higher concentrations.

Damaging Doses
"Pollutants that have been considered safe when tested at medium doses could have damaging effects at lower doses," Penn and Zala warn in their review. And conversely, toxicologists might exaggerate the risks posed by higher doses.

Other behavioral biologists back the authors' call for biologists and toxicologists to work more closely to determine the scale of the problem. "It's been decades since the first evidence appeared that chemicals in the environment can influence behavior," says John McCarty of the University of Nebraska in Omaha, who researches the impact of pollutants on birds.

"It seems to me that this body of evidence was pushed to the background while most environmental scientists and regulators focused on mortality and cancer rates [caused by endocrine disruptors and other pollutants]."

The US Environmental Protection Agency says it cannot provide a detailed comment on the research, but promises it will investigate further. "We'll review these two scientific articles as we continue to develop an endocrine screening and testing program," a spokeswoman told New Scientist.

Geoff Brighty, ecosystems science manager at the UK Environment Agency, agrees that studying the effects of chemicals on animal behavior should be given a higher priority. "It is becoming recognized that behavior is important to look at to make sure a chemical is safe, and we ignore it at our peril."