Monday, December 14, 2015

Study shows how algal toxin damages sea lions' brains and behavior

Neuroscientist Peter Cook with one of the sea lions that served as a control during the study. (Photos courtesy of the Marine Mammal Center.)

By Carol Clark

A study of wild California sea lions provides the first neurobiological evidence for how a naturally occurring algal toxin affects both the brains and behavior of the animals, leading to significant deficits in spatial memory. The journal Science is publishing the findings, showing how domoic acid damages the sea lions’ hippocampus and disrupts an important neural network.

“We were able to correlate the extent of the hippocampal damage to specific behavioral impairments relevant to the animals’ survival in the wild,” says lead author Peter Cook, a post-doctoral fellow in the Center for Neuropolicy at Emory University. Cook conducted the sea lion research while a graduate student at the University of California, Santa Cruz, and he is continuing to expand on it at Emory.

“Our research provides a way to model the behavioral and biological effects of this toxin in a large-brain mammal,” Cook says. “Better understanding of these effects may also help us identify subtle effects in humans that may be at risk.”

Although cases of fatal human domoic acid poisoning are rare, due to careful monitoring of fisheries, it is unclear if there are effects that go undetected in communities that eat unmonitored seafood.

"Sea lions are like sentinels of ocean health," Cook says, "because when they are in distress, they will almost always swim to shore."

Warming oceans and agricultural runoff may be two factors contributing to an increase in harmful algae blooms, including the planktonic algae Pseudo-nitzschia. The algae produces domoic acid, a potent neurotoxin. During large blooms, the acid can become concentrated in the tissues of shellfish and in fish that feed on the algae. Sea birds and marine mammals that consume these marine organisms can then become poisoned.

Whales and dolphins are also likely impacted by domoic acid, Cook says, although they are more difficult to study than sea lions. “Sea lions are like sentinels of ocean health,” he says, “because when they are in distress, they will almost always swim to shore. We can measure their neurobiology in ways that we can’t in other animals that may also be in distress.”

Wildlife suffering from domoic acid toxicity can display a range of odd behaviors, including seizures, lethargy, disorientation, excessive friendliness or aggressiveness. The condition is often fatal.

Poisoned birds spawned a film.
In 1961, Monterey Bay summer resident Alfred Hitchcock was captivated by reports of frenzied sooty shearwaters. It was a mystery why flocks of the birds were seen regurgitating anchovies, flying into objects and dying in the streets. The incident inspired one of Hitchcock’s most famous films, “The Birds.”

Scientists did not connect domoic acid toxicity to strange behavior by wildlife in the region until the 1990s, when masses of brown pelicans became disoriented and died.

This year, the west coast experienced a massive algae bloom, the largest ever recorded. It extended from Southern California to Alaska, prompting numerous closures of shellfish fisheries.

Large algae blooms attract large schools of fish that feed on them, such as anchovies and sardines. That, in turn, attracts the sea lions. “They are opportunistic feeders and they like to gorge themselves when they have the chance,” Cook says.

Prior research has characterized some of the clinical effects of domoic acid poisoning, but Cook wanted to assess the behavioral effects in wild animals and measure the correlation between the biological changes.

During a three-year period, the research team studied 30 California sea lions undergoing veterinary care and rehabilitation at the Marine Mammal Center in Sausalito. The study included animals with and without symptoms of brain damage caused by exposure to domoic acid.

The sea lions underwent behavioral tests to assess their spatial memory and brain imaging (MRI). The results documented impaired performance on short- and long-term spatial memory tasks in animals with lesions on the right side of the hippocampus. The lesions appear similar to those seen in humans with medial temporal lobe epilepsy.

While acute poisoning can cause seizures and disorientation in sea lions, brain lesions develop over time, likely as a result of the chronic epileptic condition caused by one or more exposures to the toxin, Cook says. “We don’t know how heavy the exposure needs to be, or how often repeated, to cause this kind of brain damage, and we don’t know the effects of repeated low-dose exposure.”

The team also used functional MRI to look at the effects of domoic acid exposure on important brain networks. They found that sea lions with symptoms of toxic exposure had greatly reduced connectivity between the hippocampus and the thalamus, a pathway known to be essential for the formation of episodic memory – memories of events and experiences.

“This is the first evidence of changes to brain networks in exposed sea lions, and suggests that these animals may be suffering a broad disruption of memory, not just spatial memory deficits,” Cook says.

The sea lion study provides rare experimental evidence linking a naturally occurring neurotoxic effect to behavioral impairment in a wild animal. “Nature was doing the dosing. Our study was a natural experiment, giving it ecological validity,” Cook says. “Animals are complicated and they live in complicated environments that are changing really fast in ways that can have a negative impact on a wide range of species.”

Co-authors of the study also include researchers from the University of California, Davis, AnimalScan Advanced Veterinary Imaging, Pennington Biomedical Research Center; the Marine Mammal Center and the Shedd Aquarium. The work was funded by the National Science Foundation and the Lucile Packard Foundation.

A sea lion that bops to a musical beat

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