"These juvenile fish on the outside look completely normal, but their hearts are not functioning properly and that translates directly into reduced swimming ability and reduced survival," Incardona said. "In terms of impacts to shore-spawning fish, the oil spill likely had a much bigger footprint than anyone realized."

The 986-foot Exxon Valdez struck a charted Bligh Reef at 12:04 am March 24, 1989, spilling 11 million gallons of crude oil. At the time, it was the largest spill in U.S. history. Oil extensively fouled shoreline spawning habitat of herring and pink salmon, the two most important commercial fish species in Prince William Sound.

Fish larvae sampled close to high concentrations of oil were found with abnormalities. Little was known in the early 1990s, however, about effects of low-level crude oil exposure on fish in early life stages, according to the study.

Pink salmon declined but recovered. The herring population collapsed three to four years after the Exxon Valdez ran aground and the role of the spill, NOAA Fisheries scientists acknowledged, remains controversial.

The silvery fish is a key species because it is eaten by salmon, seabirds and marine mammals from otters to whales. Four years after the spill, the estimated herring population based on modeling shrunk from 120 metric tons to less than 30 metric tons.

For their study, the scientists temporarily exposed herring and salmon embryos to low levels of Alaska North Slope crude oil before placing them back into clean water. They found that thresholds for harm were "remarkably low," suggesting that the effects of spilled Exxon Valdez crude was much greater than previously thought.

According to water samples collected in Prince William Sound during the 1989 herring spawning season, 98 percent of the samples had oil concentrations above the level that caused heart development problems among herring in the study.

Scientists used swimming speed as a measure of cardiorespiratory fitness. Fish exposed to the highest levels of oil swam slowest, likely making them easier targets for predators, the scientists said.

"We now know the developing fish heart is exquisitely sensitive to crude oil toxicity, and that subtle changes in heart formation can have delayed but important consequences for first-year survival, which in turn determines the long-term abundance of wild fish populations," said Nat Scholz, leader of the NOAA's Northwest Fisheries Science Center in Seattle.

If most herring spawned in 1989 near oiled shorelines developed heart defects, the mortality when they were juveniles would have resulted in far fewer adults joining the population. That could have explained the collapse four years after the spill when those adults would have matured and spawned.

Incardona said the findings should contribute to more accurate assessments of the effects of future spills.

The Associated Press