Traces of viral activity have been found in a mysteriously dwindling population of Pacific salmon, hinting at an explanation for deaths that have so far baffled scientists.

In fish returning to Canada's Fraser River, site of the die-off and home to one of North America's last great sockeye salmon runs, researchers discovered patterns of gene expression usually seen when a body fights a virus.

The findings are not conclusive, and pose many as-yet-unanswered questions. "This is the discovery stage," said Scott Hinch, a University of British Columbia salmon ecologist. "But it raises all kinds of concerns."

The importance of salmon in the Fraser and elsewhere isn't only in the intrinsic marvelousness of creatures that are born far from the sea, spend adulthood thousands of miles away in the open ocean, and return in a final blaze of upstream glory to spawn and die in the waters of their birth.

The Fraser River's wild salmon fishery is worth about $1 billion annually. And that's just the obvious value. Salmon migration is also a physical circuit to the sea, each body a mass of nutrients carried from ocean to continental interior, scattered by scavengers across the land.

Some researchers think the Pacific northwest's forests are so lush not just because of the region's climate, but because its soils were fertilized for thousands of years by salmon bodies – an extraordinary line of natural credit, now threatened by dams and overfishing.

Unlike other major river systems on North America's Pacific coast, however, the Fraser is largely undammed. Even as other Pacific salmon populations vanished or entered boom-and-bust cycles typical of ecosystems on the brink of collapse, its own populations persisted. Until the early 1990s, about 8 million sockeye salmon returned each year to spawn. Then their numbers started drop.

In some years, half of the Fraser's returning sockeye die before spawning. In other years, mortality is closer to 95 percent. "The causal mechanisms of this premature mortality have eluded multidisciplinary research by scientists and fisheries managers," wrote Hinch and his colleagues, led by biologist Kristina Miller of Fisheries and Oceans Canada, in a Jan. 14 Science paper.

In less academic terms, the fish are dying, and nobody can figure out why.

Five years ago, the researchers noticed that some Fraser sockeye appeared to show unusual signs of physiological stress while at sea. In the new study, they take that work to the genomic level. Salmon were caught, biopsied and tagged with radio transmitters in the ocean, about 120 miles from the Fraser; at the Fraser's mouth; and again on their spawning grounds. For each stage, the researchers could look for patterns in gene expression, then see if they tracked with differences in fate.

A pattern stood out. Many of the fish displayed high activity in a set of genes typically activated in response to viral infection. When this genomic signature was found in ocean fish, they were 13.5 times more likely to die before reaching the Fraser. When the signature was found in fish tagged in the river, they were 50 percent more likely to die before reaching their spawning grounds. In fish tagged on their spawning grounds, those with the signature were 3.7 times more likely to die without mating.

"It's excellent science," said fish microbiologist James Winton of the U.S. Geological Survey, who was not involved with the research. "This appears to be quite important." Winton applauded the researchers' approach, which had never before been used in salmon, a species for which researchers only notice the most obvious diseases.

"The fact that, within the physiology of these fish, you can see signs of who is likely to make it and who won't, is amazing," said Michael Webster, a program officer at the Gordon and Betty Moore Foundation's Wild Salmon Ecosystems Initiative.

However, though a virus is the most likely culprit, it hasn't yet been isolated. The findings open up a range of new questions, said each of the researchers: If the pattern is indeed caused by a virus widespread in the Fraser, where did it come from? Was it introduced, just as infectious hematopoietic necrosis – a lethal virus endemic in Pacific salmon – has been transferred around the world? If it was always there, did it suddenly evolve into a more virulent form? Or is something else exacerbating its effects?

The researchers suspect climate has a role in the answers to some of these questions. In the last 40 years, the Fraser's waters have warmed by about 4 degrees Fahrenheit, with most of that coming in the last 15 years. "In some cases, that temperature alone is pushing fish stocks to the edge," said Hinch.

Heat and stress can weaken fish, making them more vulnerable to disease. Changing temperatures also change the ranges of microbes and parasites, allowing them to move into new regions. Over the last decade, the Yukon River has been invaded by Ichthyophonus, a parasite that threatens the river's Chinook salmon population. It's believed to have spread because of changing temperatures.

"We use the term emerging diseases. In humans, it's the SARS coronavirus, or avian flu. They also occur in fish. Part of [their increasing incidence] is due to the fact that more people are looking, with better tools. Part of it is due to us moving pathogens around the globe. And part of it due to increasing stress on these animals," said Winton. "At some point, we're going to add the last straw."

Images: Kristina Miller.

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Citation: "Genomic Signatures Predict Migration and Spawning Failure in Wild Canadian Salmon." By Kristina M. Miller, Shaorong Li, Karia H. Kaukinen, Norma Ginther, Edd Hammill, Janelle M. R. Curtis, David A. Patterson, Thomas Sierocinski, Louise Donnison, Paul Pavlidis, Scott G. Hinch, Kimberly A. Hruska, Steven J. Cooke, Karl K. English, Anthony P. Farrell. Science, Vol. 331 No. 6014, January 14, 2010.