Some fish are less capable of adapting their blood flow to rising temperatures when inhabiting oxygen-poor waters, according to a new study in sablefish, suggesting that as oxygen depletion continues to occur due to natural and human influences, many fish may face a higher risk from heat waves caused by climate change.

The study, published March 9 in Proceedings of the Royal Society B, is the first to examine the effects of long-term exposure to low oxygen levels, or hypoxia, on fishes' ability to adapt to rapid warming.

Most creatures need more oxygen when in higher temperatures to fuel sped-up reactions in tissues, according to Kurt Gamperl, a professor of ocean sciences at the Memorial University of Newfoundland and the paper's senior author. Fish normally adapt to warming waters by increasing their heart rate to transport oxygen through their blood more quickly.

But little research has investigated how fishes' tolerance to heat is affected by hypoxic waters, which can be created by rising sea temperatures or more acutely by nitrogen-rich runoff from rivers. Lead author Robine Leeuwis, a Ph.D. student studying fish physiology at the Memorial University of Newfoundland, said one question her team had was whether fish in low-oxygen waters would be more prepared for heat waves. 

"We wondered if acclimation to low oxygen levels, if this could potentially improve their ability to cope with high temperatures," Leeuwis said. In a phenomenon known as cross-tolerance, "An animal, when it is exposed in the long term to a particular environmental stressor, it may actually help it deal with another stressor."

In the new study in sablefish, which live in a wide range of oxygen levels and temperatures across the North Pacific, this turned out not to be the case.

For four or six months, the fish lived in hypoxic water with oxygen levels about 40% of maximum saturation, enough to strain their cardiovascular system but well above dangerous or lethal levels. They were then placed in fully oxygenated water for two days before oxygen concentration was quickly dropped back to 40% and temperature was subsequently raised to their maximum tolerance.

Cardiovascular and blood samples taken throughout the experiment showed that the sablefish's heart rates slowed when oxygen lowered — and slowed again when temperature was raised, lowering oxygen transport and contradicting expectations. The amount of blood moved per heartbeat increased slightly but did not offset the reduced oxygen circulating through the fish.

In another experiment, the researchers raised other sablefish in water with normal oxygen levels and exposed them to similar hypoxic and high-temperature conditions. This second set adapted to the warmer waters much more effectively, with the fish doubling their heart rate and rate of pumping blood, as expected.

"The first experiment was really designed to ask the question, 'When oxygen levels are low, how does that affect thermal tolerance, and if we acclimate animals to low oxygen, does that improve their ability to tolerate high temperatures?'" Gamperl said. "In that study we found that the sablefish was not able to increase heart rate when hypoxic, which is a very strange result."

As ocean heat waves are expected to become more frequent and extreme due to climate change, populations of fish in low-oxygen waters could be more vulnerable to rapid die-offs. Gamperl pointed to the 2.6 million salmon that died off the coast of Newfoundland in 2019, killed by a temperature spike in waters about 60% to 70% saturated with oxygen.

"It tells us that we have to be a lot more cautious when it comes to making predictions of the impact of climate change on fish," Leeuwis said. "We have to also consider the impact of hypoxia and not just temperature alone."

In research that has not yet been published, the Newfoundlander scientists ran similar tests on salmon and produced the same results, according to Gamperl. That indicates that the limiting effect of hypoxia on heat tolerance occurs in a broader range of fish and not only the unusually adaptive sablefish.

"Those two studies combined would indicate that fish are much more susceptible to climate change, given that hypoxia and high temperatures do co-occur," Gamperl said.

Further, the sablefish experiments raise questions about what mechanism is causing hypoxic fish to lower their heart rate in conditions where their body needs more oxygen, according to the researchers.

Leeuwis and Gamperl are also interested in running similar tests on fish swimming more quickly as they might while migrating, rather than staying at rest like the fish in this study. Leeuwis speculated that increased muscle activity and contractions could return blood to the heart more quickly.

The study, "Research on sablefish (Anoplopoma fimbria) suggests that limited capacity to increase heart function leaves hypoxic fish susceptible to heat waves," published March 9 in Proceedings of the Royal Society B, was authored by Robine Leeuwis, Fábio Zanuzzo, Ellen Peroni and Kurt Gamperl, Memorial University of Newfoundland.