Veterinarian documents first freshwater toxin poisoning
of a marine mammal
posted November 1, 2010
Dr. Melissa A. Miller discovered a killer in her laboratory. The question now is how to prevent it from striking again.
A wildlife pathologist with the California Department of Fish and Game, Dr. Miller first began noticing a rash of mysterious southern sea otter deaths in 2007.
"The most striking thing about these animals was how jaundiced they were," Dr. Miller recalled about the necropsies she performed. "Even the whites of their eyes were bright yellow, and the liver would fall apart in my hands."
"(Southern sea otters are) a very interesting and unique marine mammal species, and those interesting and unique attributes are, in part, what make them a threatened species."
DR. MELISSA A. MILLER, WILDLIFE PATHOLOGIST, CALIFORNIA DEPARTMENT OF FISH AND GAME
Since Dr. Miller's discovery, the outlook for the southern sea otter has grown worse. In August the U.S. Geological Survey announced a decline in the southern sea otter population for the second year in a row. The agency estimates the current number of otters at 2,711—a 3.6 percent drop for the overall population and an 11 percent drop in the number of otter pups, compared with 2009 numbers.
"A number of human and natural factors may be influencing this trend, and we are working to better understand what those are," Tim Tinker, PhD, the lead survey scientist, said.
At first Dr. Miller suspected the culprit was Leptospira spp, since leptospirosis is common among sea lions that share the same coastal waters as the sea otters. But all the tests for the bacterium came back negative.
So what was killing these affable marine mammals?
After ruling out leptospirosis, Dr. Miller began to run through a long list of other potential causes.
One by one, she eliminated the possibilities, including poisonous mushrooms and iron toxicosis, until she finally arrived at microcystin toxicosis, caused by cyanobacterium of the genus Microcystis and more widely known as blue-green algae. Sure enough, liver samples tested positive for the toxin.
What Dr. Miller found strange was that the microcystin toxin is produced by organisms typically found in warm, stagnant, nutrient-enriched fresh water. How were sea otters ingesting lethal doses of the toxin?
Dr. Miller made a few calls and learned that an unusually high number of Microcystis blooms had been seen in lakes and estuaries throughout California, including Pinto Lake, located approximately six miles inland from Monterey Bay.
A technician she dispatched to collect samples from Pinto Lake reported back, "This is gnarly," referring to the large green algae chunks floating in the water, Dr. Miller said. The water samples tested positive for some of the highest Microcystis concentrations seen not only in California but throughout the entire country.
Next, Dr. Miller wanted to know whether it was biologically plausible for the toxin to make its way from the lake into the ocean. It was. "We tested the lake, the creek connecting it to river, and the river connecting it to ocean," she said. "We documented the presence of the toxin and bacterium that produces it all the way down to within one kilometer of the ocean, and that was during the dry season."
The final part of the mystery was determining how, after the toxin made its way downstream, it got into the sea otters. Dr. Miller's hypothesis was the otters' food was the source of their exposure. This is where the sea otter's distinctiveness among marine mammals comes into play.
"They're a very interesting and unique marine mammal species, and those interesting and unique attributes are, in part, what make them a threatened species," she explained.
For instance, sea otters tend to feed along the shoreline on bivalves such as clams and mussels—all filter feeders capable of concentrating both biological and chemical pollutants in their digestive tissue. And because sea otters don't develop a layer of insulating blubber as do seals, dolphins, and other marine mammals, they have a high metabolic rate that requires them to eat a lot to maintain body heat. In human terms, if a 160-pound human ate like a sea otter, he or she would have to eat 40 pounds of hamburgers daily to stay healthy, according to Dr. Miller. That caloric intake increases if the otter is nursing, pregnant, or sick.
"You can see all those attributes contribute to sea otters being highly sensitive environmental sentinels," she said.
To test her hypothesis, Dr. Miller exposed a variety of foods consumed by otters and people for four days to microcystin from Pinto Lake. What she discovered is that clams, mussels, snails, and oysters were very adept at picking up the toxin when present in seawater. She also found that microcystin was stable in seawater and, once the invertebrates took up the toxin, it tended to persist in their digestive systems for at least three weeks.
"All of these things support the hypothesis that this is how the otters are being exposed to the toxin," Dr. Miller said. Her findings, which documented the first case of a freshwater toxin poisoning a marine animal, were published in the Sept. 10 edition of PLoS ONE, one of the online journals published by the Public Library of Science. Twenty-one sea otter deaths have so far been attributed to microcystin intoxication.
Although it's not known for certain, it appears that the sea otters are most at risk of microcystin poisoning in the fall when the rainy season flushes these toxins into the ocean. Dr. Miller says state and local officials are working now to identify what's triggering these algae blooms, with the goal of preventing them.
"People obviously do care and are working on this," Dr. Miller said.