Mar 12, 2021 8:00 AM

Ocean Acidification Could Make Tiny Fish Lose Their Hearing

Their inner ears turn wonky when they grow up in carbon-rich water, which could keep juveniles from finding their way to the reefs. That could mean trouble.

An immobilized fish lay between Craig Radford's fingers. The several-week-old Australasian snapper, no longer than a pinkie nail, rested flat on a slab of modeling clay, held down by small staples—“as someone would strap you down on an ambulance bed to hold you there,” says Radford. He stuck tiny electrodes on the fish’s head, then submerged it in a tank and switched on an underwater speaker. It was time to test its hearing.

“If you actually put your head underwater and take the time to listen, it's amazing what you'll hear,” Radford says. “From whales to fish to crustaceans—sound plays an important role in many, many different species’ life strategies.”

But Radford’s experiment wasn’t due to curiosesity about what the world sounds like to fish. He was worried about how well they could hear it.

Life-forms lurking in Earth's oceans depend a lot on what humans do above the surface. After we burn the carbon-rich fuels that nations mine, chop, and slurp out of the ground, they meander into the atmosphere as pollution, such as carbon dioxide. Increased CO₂ in the atmosphere leads to more dissolved CO₂ in the oceans, too, where it acidifies plant and animal habitats. In some cases, the consequences make intuitive sense: A more acidic ocean corrodes coral reefs and the symbiotic microorganisms hanging around them. But other effects are less straightforward, and Radford and his team found a weird one: The CO₂ levels can morph the inner ears of fish, leading to hearing loss.

In a new study, a team of researchers from the University of Auckland, New Zealand, and James Cook University in Australia used neural electrodes and a micro CT scanner to measure the first evidence of what happens to reef fish hearing when larvae develop in a more acidic ocean. They found that the juvenile Australasian snapper can be roughly 10 times less sensitive to sound—a potentially fatal blow to animals that rely on hearing to find their way home. The team’s result highlights a surprising example of knock-on effects of atmospheric change. The work was published last week in the Proceedings of the Royal Society B.

“It's not intuitive that fish would not be able to hear, or not be able to smell, or not be able to behave correctly,” says Sean Bignami, a biologist running Concordia University Irvine’s Marine Lab, who was not involved with the study. Bignami studies how acidification affects ocean life, and he studied fish inner ears in his doctoral work. “I think it's fascinating,” he says of the new results.

Many reef fish are actually hatched in the open ocean, and the juveniles must swim back to the reef where they will make their home, Radford says. “A lot of work has shown that sound is an orientation cue to find their way back,” he says. Messing with that sense of hearing can threaten a species’ survival.

Sound is a major concern for marine ecologists studying how human behavior in the air-breathing world affects our finned kin. Warming oceans make snapping shrimp snap louder, creating noisy interference for their underwater neighbors, and an enormous review published in Science in February, on which Radford was a coauthor, concluded that human noise has made the “soundscape” unbearable for sea creatures. Noise pollution drowns out whale sounds, for instance, which complicates socializing and mating.

Fish, including the Australasian snapper, use sound to communicate, procreate, and orientate. Some use it to attract mates or synchronize egg and sperm release. Some baby fish use it to find suitable reefs to live in.

Ocean acidification challenges matters through the fish’s anatomy. Studies accumulating over the past dozen years show that the hard stones making up fish “ears,” called otoliths, grow abnormally large when larvae develop in more acidic waters. A previous study, coauthored by Bignami, actually predicted this would improve hearing. But models are only as good as the data, and the data was limited. So Radford’s group wanted to test the actual neurological effect in fish. “What does that mean in terms of how those ears function?” Radford says. “We really didn't know.”

Cracking that mystery intrigued Radford, who specializes in sensory physiology and, in particular, hearing. Whether through air or water or the layers of drywall that separate you from your upstairs neighbor, sound travels when vibrating particles nudge each other back and forth. The particles bump each other with the same frequency as the original sound. On the receiving end, they thump ear drums, oscillating between maximal thumps and minimal thumps—high pressure and low pressure. We think of sound as these pressure waves because it’s how we hear and how our speakers and microphoness function: In our ears, pressure waves rattle small bones, vibrating fluid in the cochlea and causing nerves to fire. Fish inner ears are different. “They basically work as accelerometers,” Radford says. Fish otoliths don’t sense pressure waves, they sense particle motion.

Photograph: Craig Radford/University of Auckland

Fish bodies are about the same density as seawater, but their otoliths are three or four times denser. When sound hits a swimming fish, its body moves in tandem. “The denser otoliths lag behind,” Radford says. Their brains measure the lag between otolith and body, and register that sensory input as sound.

Radford’s team thought that because ocean acidification morphs otoliths, it probably changes hearing as well. They collected Australasian snapper eggs and began their test 21 days after the larval fish hatched. To tease out what acidification does, they exposed 10 larva to typical CO₂ concentrations, and 10 to elevated CO₂. At 42 days, the larvae had all turned into juvenile fish. Radford next wanted to measure how their otoliths had developed differently in each condition, and what that meant for their hearing.

Bones and stones show up well in typical CT scans, and labs even have “micro” CT scanners that provide enough resolution for small creatures. But these otoliths were tiny stones in already minuscule fish. To keep the small parts stable enough to capture a clear image, Radford’s team had to get creative—with a straw. “We basically put the fish in the straw and we capped the ends with a piece of polystyrene,” he says. The tiny foam-stuffed tube held the baby fish in place and kept it free of air that would muddy up measurements.

As expected, the otoliths in fish exposed to higher carbon dioxide levels were slightly larger—Radford wasn’t surprised. “More important,” he adds, “the symmetry between the left and right side were different.”

Symmetry is vital for two-sided animals such as fish and humans. “If you look at someone's face, most people are symmetrical, the left side matches the right side. It's the same with all human sensory systems,” Radford says. Fish brains depend on symmetrical anatomy to compute their perception of hearing from the raw sound. If you ditch that symmetry, the mental math changes—and the fish’s hearing becomes less sensitive. “If you've got otoliths that are a different shape,” Radford says, “then one is going to sense something different to the other, which is going to make any form of sound localization more difficult.” If you've ever lost your balance because you have water clogging one ear, you've experienced something similar.

Radford’s team actually measured how ocean acidification could weaken hearing. Radford placed tiny sensors on each fish immobilized in the modeling clay, right near their brainstems. Then once the fish were back in the tank, the researchers played tones and measured “auditory evoked potentials”—the electrical signals the brain receives.

“We found that the low-frequency part of the hearing dropped down,” Radford says. At frequencies between 80 and 200 hertz, hearing sensitivity collapsed roughly 10 decibels. Most vocal fish communicate at frequencies between 100 and 300 Hz, a deep hum to a mild ooo. And decibels run on a logarithmic scale: A 10 decibel decrease means a tenfold decrease. “It's bad news, particularly for fish, if they can't hear at these low frequencies,” Radford says.

Bignami is taking the model-defying results of the new study in stride. A bigger otolith should make hearing more sensitive, as his model found, but the surprising contribution from asymmetry between left and right otoliths ends up being way more important. “Measuring actual neurological signals in juvenile fish is really difficult to do,” he says of the new study. “It's quite convincing. They're observing a pretty clear change here.”

The full consequence on fish behavior will result from a combination of overgrown otoliths, asymmetric anatomy, and neurochemical effects. Ocean acidification makes some fish brains less receptive to a neurotransmitter controlling impulsive behavior. (In one study, larvae raised in acidified waters swam toward the smell of predators.)

“It shouldn't be overlooked that this is looking at the relationship at a really critical life stage,” says Sara Shen, a marine scientist who now works for an environmental consulting firm that was not involved with the study. Shen’s previous research showed the connection between otolith size and a type of balance called vestibulo-ocular reflex in a sensitive transition point for fish larvae. Radford’s chosen period, where young fish are settling on reefs, is very important for maintaining their populations. “This is really great work,” she says.

So what does this experiment tell us about how climate change is affecting reef fish? The tenfold drop in hearing was observed among fish exposed to a 120 percent increase in dissolved carbon dioxide from 450 to 1,000 micro-atmospheres of pressure in water. Since CO₂ is a dissolved gas, this value represents the pressure it would have in an otherwise empty container, where 1 million micro-atmospheres equals normal air pressure. Such a big average concentration increase won’t happen in surface waters in the next few years, although it fits longer-term trends if CO₂ emissions continue unabated.

But even a smaller drop in hearing acuity, caused by milder acidification, would still be significant. Deafened juvenile fish could struggle to find reefs when migrating after hatching in the open ocean. If they can’t settle, they can’t survive and spawn. And those fish play an important role in maintaining reefs. Predatory reef fish, for example, eat herbivores, which in turn keep algal growth in check. Overgrown algae smothers coral. The coral dies and erodes. Fish shelters and egg-laying surfaces vanish along with it. “That ecosystem disappears,” says Yvonne Sadovy, a marine biologist at the University of Hong Kong who was not involved with the study.

Sadovy likens reef life to a bustling urban city. “There's just this incredible balance, the way different species live and depend on each other,” she says. “It seems chaotic, but it's actually not. Everything and everybody has its place, and its job, and its part of the functioning of the city. If you take out parts of those functions—like, if you took out all the buses and the trains— then it's going to affect the functioning of other aspects of the city.”

People in many economically developing countries also rely on these reefs for food and their livelihoods. People living in the Maldives, for example, source 77 percent of their dietary animal protein from reef fish. With these marine environments already under pressure from eroding corals and overfishing, hearing damage just makes matters worse for reef fish populations.

Sadovy says people don’t always realize how important reef fish and their fisheries can be. She published a report in 2019 that details how undervalued reef fish are as a natural resource, calling for more resilience in how governments maintain fish populations. “Fishing in small-scale communities, in the tropics and the subtropics, supports millions of people,” Sadovy says. “In terms of the economic value, they're enormous; in terms of the food value, they’re enormous; livelihood and just supporting communities—seafood is enormous.”

Of course, lab experiments are not experiments in the wild. Bignami points out that species can adapt over generations. “We can't make any conclusions that are too overly confident about how this is going to play out in the wild,” he says.

Still, that these effects are even possible is worth knowing on its own, says Sadovy. “Many people feel maybe that the seas are so big, and we are so small, that we can't possibly have a major impact on the species and on the seas themselves,” Sadovy says. “But actually we are having those impacts. We really are. We know this.”

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