Researchers have found that increased carbon dioxide in the ocean interferes with gilthead seabreams' sense of smell both directly and indirectly — by reducing the sensitivity of their olfactory neurons and by acidifying the surrounding water.

The study, published March 3 in the Journal of Experimental Biology, suggests that the dangers to marine life posed by climate change are more complicated than previously understood.

"As humans thinking about senses, we're highly visual and highly auditory, so we forget how important olfaction is in other animals," said Peter Hubbard, a researcher at the Center of Marine Sciences of Universidade do Algarve in Portugal. "With fish and other marine animals, having slightly less sensitive sense of smell will [cause them to] have more difficulty finding food, or difficulty finding their home range, or avoiding predators. All these things are compounded with all the other changes that humans are making to the sea."

Fish are able to smell when odorant molecules pass across their olfactory epithelium, which lines their nasal cavities. While this aspect of fish olfaction, or sense of smell, is similar to that found in other animals, including humans, the key difference in fish is that it must take place entirely in an aquatic environment.

This means that changes in a fish's ability to smell can be caused by changes in the chemistry of the surrounding water. For example, fish olfaction has been shown to be interrupted by 4-nonylphenol, a common environmental contaminant found in detergents.

Carbon dioxide in the ocean is increasing at an alarming rate as a result of climate change. According to the U.S. National Oceanic and Atmospheric Administration, the global ocean absorbed 34 billion metric tons of carbon from the burning of fossil fuels between 1994 and 2007, a fourfold increase over the previous century.

While this study is not the first to examine the role that carbon dioxide plays in fish olfaction, it is among the first to separately study the effects of both ocean acidification and increased carbon dioxide concentration. While these effects are intertwined, carbon dioxide alone does not make the ocean more acidic. It must first react with water to form carbonic acid as part of the larger carbon cycle.

"In nature, CO₂ dissolves into the ocean to cause a reduction in pH, so it's artificial to try and separate them," Hubbard told The Academic Times. "But we wanted to see whether it was the CO₂ itself or the reduction in pH that causes the problem."

The motivation for this "artificial" separation of variables emerged from an unanswered question in a previous study conducted by Hubbard and colleagues. In that study, they demonstrated that increased pH in the water adds protons to both the fish's olfactory receptors and to the odorant molecules that the fish smell. This changes the shape of each molecule and makes them less likely to bind, dulling the sense of smell.

"We found that this could explain some, but not all of the loss of olfactory sensitivity," Hubbard said. "So there's something else going on."

This led the researchers to hypothesize that the presence of carbon dioxide in the atmosphere can directly influence fish olfaction, even without a change in overall ocean pH.

They tested their hypothesis in the lab by using electrodes to monitor the activity of the olfactory rosette of gilthead seabream in water with different levels of acidification, as well as with different levels of carbon dioxide. The fish is found in the Mediterranean and on the Eastern Atlantic coast.

Hubbard explained that using these electrodes rather than monitoring fish behavior helped the team avoid some of the pitfalls of previous experiments in fish olfaction, namely that behavioral experiments are somewhat unpredictable and difficult to reproduce.

The team found that both carbon dioxide concentration and ocean pH interfered with fish olfaction independently of one another.

"It was a surprise to me to see that by simply increasing the CO₂, and then readjusting the pH back to normal, we did get a reduction in olfactory sensitivity," said Hubbard. "I wasn't really expecting that."

While the specific mechanism by which carbon dioxide on its own reduces the sensitivity of fish smell warrants further study, the researchers hypothesize that the gas diffuses from the ocean water into the intracellular space of the olfactory neurons and causes the water in that space to become acidified as well, compounding whatever interference the surrounding pH may be causing.

The researchers will continue to work on pinpointing precisely what is occurring on a molecular level in fish as carbon dioxide levels increase. Hubbard also emphasizes the importance of looking at multiple factors when assessing the dangers of climate change and carbon pollution, as well as the importance of people doing their part in reducing these dangers.

"On one level, the message is to stop polluting so much CO₂. Take your cycle. Take the bus," he said. "On another level, think more about the marine environment in general. Take care of it. It is the least affected human environment on the planet."

The study, "Independent effects of seawater pH and high PCO2 on olfactory sensitivity in fish: possible role of carbonic anhydrase," published March 3 in Journal of Experimental Biology, was authored by Zélia Velez, Rita A. Costa, Wenjing Wang and Peter C. Hubbard, Universidade do Algarve.