Losing the scent of danger
Copper runoff in streams damages young salmon’s sense of smell, making them more vulnerable to predators.
Fish are like swimming bloodhounds. Swirling water through their noses, they pick up minute chemical cues that can guide them thousands of miles to spawn in just the right spot, or can sound an alarm that tells them to hide from oncoming predators.
But research published today on ES&T’s Research ASAP website (DOI: 10.1021/es062287r shows that copper entering streams from urban and agricultural runoff can damage salmon’s fine sense of smell. This disrupts their predator-avoidance behavior and puts them at risk of being gobbled up. Young fish are especially vulnerable, because they’re snack-sized for many predators, such as kingfishers and trout.
The problem extends beyond copper, and even beyond fish. Greg Pyle of Nipissing University (Canada) says he and other toxicologists are starting to refer to the loss of animal sensory systems as “the hidden global change”. Pyle has studied animals at three levels of the aquatic food chain, from leeches that “live in the muck” to top predator fish. “With every organism we look at, and every metal we’ve considered, we see the same effects,” he says. “Very low concentrations of metals can knock out the chemosensory system.”
Storm water rinses copper into streams from roadways and agricultural fields, where it accumulates from sources including pesticides, vehicle exhaust, and tiny particles ground off brake pads. “The neurons in a fish’s nose are in direct contact with the water, so the nose would be the first part in contact with the contaminants,” says lead author Jason Sandahl, who completed the work as a graduate student at Oregon State University. “One thing that surprised me was how sensitive their olfactory systems are—they’re much better than dogs’,” he says. The team studied coho salmon and found that they could detect pheromones emitted from a piece of fish skin 1 square millimeter in size—smaller than a grain of rice—in 100 liters of water.
The study combined observations of fish behavior with physiological measurements of nerve signals measured by placing sensors in fish noses. The team demonstrated in earlier work that copper damages salmon’s delicate nose tissue and disrupts olfactory nerve signaling.
Sandahl says the research points out the need for more behavioral studies in toxicology. “Clearly, simple mortality tests are not good enough anymore,” he says.
“For the last 30 years, we’ve known that olfaction could be affected, but the question was, what does it mean when a fish can’t smell? This is the first study to link that to a specific behavior,” says Scott Hecht, an ecotoxicologist in the Office of Protected Resources at the National Oceanic and Atmospheric Administration (NOAA). The next step, he says, should be to learn whether these behavioral changes translate to real losses of juvenile salmon in wild populations.
In one video of the study, a young coho salmon darts madly around an aquarium filled with clean, copper-free water until a researcher drips in a solution made from a tiny piece of torn fish skin. Suddenly, the salmon sinks to the bottom of the tank and hovers in a fish version of a doggy paddle. Its nose is telling it that another fish has been injured, so a predator must be nearby. In the wild, bears and other fish-eaters look for movement, so this stop-and-drop technique helps salmon avoid notice.
Meanwhile, a salmon in another tank has been swimming for 3 hours in water spiked with just 10 parts per billion copper, a level commonly found in streams after storms. When the skin solution hits the water, this fish seems oblivious. Instead of lying low, the salmon just keeps speeding along. In the real world, this can mean becoming someone else’s dinner.
And that’s a real problem. Today, 26 different populations of salmon are listed as threatened or endangered under the U.S. Endangered Species Act. Coho are particularly vulnerable to copper in streams, because they spend the first year of life in freshwater before heading to sea.
“It’s possible that the risk is underestimated, because this is just one of many chemicals that could influence behavior,” says Richard Di Giulio, an ecotoxicologist at Duke University. However, he adds that “the largest uncertainty would be how this would play out in real-world surface waters with materials that could potentially reduce the bioavailability of metals, like dissolved organic matter.”
Study coauthor Nathaniel Scholz of NOAA’s Northwest Fisheries Science Center notes that the team is currently doing experiments using artificial freshwater. So far, he says, the preliminary results show that fish are still affected by copper even in the presence of materials that bind metals.
The coho were able to regain their sense of smell within hours after short exposures to low doses of copper, as receptor neurons recovered. However, other research has shown that these neurons can die at higher concentrations. “When neurons in the nose die, they can still regenerate, but it can take several weeks to a month to regrow,” Sandahl says, which could be too late for a fish that needs to hightail it to safety.
