Try, for a moment, to be a fish. As you swim through dim waters, you see shapes moving past and watch for threats. You hear other animals calling or producing rasps and crackles by scraping together rigid body parts. The water is a tapestry of smells that reveals predators and potential mates, food, and the route home.
Now, imagine that nothing makes sense—the tapestry has unraveled. Smells still reach you, but their meanings are muddled. You listen for calls from your kin, but all you hear is the roar of a passing boat. You can't tell whether that looming shadow is a friend or foe.
When many people think of threats to the world's fish, overfishing or vanishing reefs might leap to mind. Increasingly, however, scientists also worry about a subtler danger: how human activities might interfere with the senses fish use to perceive the world. Noise from ships and construction, murkier waters caused by pollution, and rising ocean acidification from the buildup of atmospheric carbon dioxide (CO2) are all possible culprits. In laboratories and in the wild, scientists study exactly how those factors might affect a fish's ability to communicate, navigate, and survive.
The studies face both logistical and conceptual challenges. Observing the behavior of fish in the vast sea is nearly impossible, but a laboratory aquarium is a far cry from their natural environment. And we can't know exactly what seeing, smelling, or hearing as a fish is like. But by drawing on tools as elaborate as simulated underwater environments and as simple as bits of thread tethering baby fish to stream bottoms, researchers are gaining a better understanding of how fish use their senses—as well as the consequences of disrupting them.
Driving the work is the concern that humans are creating a pervasive threat to the fish stocks that provide food and livelihoods for millions of people: a kind of sensory smog. Combating causes such as pollution and acidification is a staggering challenge, the scientists admit. But the stakes are high. "The knock-on implications are huge," says Jennifer Kelley, a behavioral ecologist at the University of Western Australia in Perth. When fish with compromised senses settle in the wrong homes or fail to recognize predators, the results could ripple outward "to how individuals interact and how communities operate, and the whole ecology of the system altering."
An 11-day-old clownfish, pale orange and about as long as a grain of rice, searches for a place to settle down on a reef. Its keen sense of smell helps it both navigate to a safe home and steer away from the mouths of predators.
In the wild, clownfish inhabit living coral reefs. But in behavioral ecologist Danielle Dixson's laboratory at the University of Delaware in Lewes, the habitats beckoning the fish are made mostly of wires. Dixson will use the experimental setup to study how ocean acidification could alter how fish perceive and respond to their world. (Editor's note, 7 May 2021, 2 p.m.: Since Science published this story, researchers have raised concerns about the validity of some studies of the impact of ocean acidification on fish behavior authored by Dixson. Learn more here.)
The laboratory—a converted garage with black bags taped over the windows to block bright light—holds two bays of fish tanks. A network of densely draped cables connects sensors in the aquariums to a black box on the wall, which researchers call "the brain." It helps them monitor and control water temperatures and acidity levels in each tank.
In some tanks, Dixson will keep clownfish and other species in seawater with the acidity levels found now in the ocean. In other tanks, the water will be more acidic, to mimic the ocean chemistry that's forecast for later this century if humans do not curb CO2 emissions. In both cases, conditions fluctuate during the day, as on a real reef. The researchers will look at how pH levels affect the way fish behave, interact, and respond to olfactory cues.
Dixson is building on research showing that acidification can jumble a fish's response to smells. For example, she and colleagues reported in Ecology Letters in 2010 that young clownfish raised in more acidic waters were strongly attracted to the smell of a predator, which the fish would normally avoid. In some predatory fish, acidification had the opposite effect. Dixson and co-authors found that after 5 days in water with high levels of CO2, sharks called smooth dogfish avoided the smell of their prey. Other researchers found a similar result in the brown dottyback, a reef-dwelling predator.
Acidification also seems to cause other behavioral changes. In boldness tests—in which researchers approach fish with a blunt object to make them retreat—fish treated with acidic water come back out of hiding sooner. Those fish are like angry teenagers, Dixson says. "They're really aggressive, but they really don't know what they're doing."
The problem isn't that acidified water damages fish noses, Dixson says. Instead, the issue is apparently in the brain. Multiple mechanisms may be at work. One strong possibility is that acidic conditions interfere with brain cell receptors that respond to γ-aminobutyric acid (GABA), a neurotransmitter. All vertebrates share GABA receptors, which inhibit neuron activity. They are "like the brake on electrical circuits in the brain," says biologist Göran Nilsson of the University of Oslo who, along with Dixson and others, first highlighted the potential connection between GABA receptors, fish behavior, and acidification in a 2012 Nature Climate Change paper.
Normally, when GABA binds to a receptor, it opens a channel that lets negatively charged chloride ions flow into the neuron. But that flow reverses in fish living in acidified water, studies suggest. That's because, physiologically, the fish cope with the more acidic environment by accumulating bicarbonate ions, which are basic, and by shedding chloride ions. When the channel is opened, chloride ions flow out of the neuron instead of into it, and the neuronal "brake actually becomes an accelerator," Nilsson says. That hypothesis has drawn support from studies in which researchers dose fish with gabazine, a drug that suppresses GABA receptors. After a quick dip in gabazine-laced water, formerly confused fish act normal again.
It doesn’t seem like there’s a lot of wiggle room for evolution or natural selection to take place.
Acidification similarly affects fish vision and hearing, perhaps also by scrambling GABA receptors. In one study, researchers treated young damselfish with high-CO2 water and then placed a plastic bag holding a predatory fish in their tank—so the damselfish could see the predator, but not smell it. Normally, that apparition would make the damselfish lie low. Instead, fish from acidified water ignored or swam close to the bag. In another study, researchers used an underwater speaker to play young clownfish a recording of a coral reef teeming with predators. Clownfish raised in high-CO2 water didn't flee from the sound, as they normally would.
Other researchers have found that otoliths, the little chunks of calcium carbonate in the inner ears of vertebrates, are larger than normal in some (but not all) of the fish species they raised in acidified waters. Changes to otolith size could affect fish hearing and orientation, researchers say.
Different fish species are vulnerable to different degrees of ocean acidification. In one study, researchers found that conditions mimicking an atmospheric CO2 level of 700 parts per million (ppm) addled about half of clownfish; all the fish were affected at 850 ppm. At current emission rates, fish populations could experience those levels well before the end of the century, leaving little time to adapt. "It doesn't seem like there's a lot of wiggle room for evolution or natural selection to take place," Dixson says.
A rising cacophony
It's early spring in the Atlantic Ocean, and an adult cod is journeying back to his preferred spawning grounds to find a mate. He grunts while he swims. He and the other migrating cod add their grunts to a marine cacophony: the barks, mutters, clucks, and chirps of other fish; the singing of whales; the steady munching of sea urchins below. Light rain above tinkles musically, reaching a crescendo when heavier storms pass. The noises reverberate in the cod's belly, where his balloonlike swim bladder acts as an extension of his ears.
What cod or other migrating fish are saying as they travel is not clear. They may be calling to stragglers, synchronizing migration or spawning, or establishing dominance. But clearly, the fish increasingly must compete with human noise sources such as recreational boats, commercial ships, pile driving, sonar, and deep-sea mining.
Marine ecologist Jenni Stanley at the National Oceanic and Atmospheric Administration's Northeast Fisheries Science Center and the Woods Hole Oceanographic Institution in Massachusetts has measured the impact of the added noise. She and colleagues recorded ambient underwater sounds at spawning sites for cod and haddock in Massachusetts Bay. Unlike the grunting cod, haddock produce an insistent knocking sound that can go on for hours. At times with less competing noise from vessels, the fish calls could carry more than 20 meters, the researchers reported in 2017 in Scientific Reports. But at noisier times, the calls carried only a meter or so before being drowned out.
Researchers don't know whether such interference has affected overall populations of cod and haddock. But scientists worry about subtle harms that could ultimately take a toll. "I think the critical issue … is the impact on the soundscape," says biologist Arthur Popper of the University of Maryland in College Park. At least 800 fish species make sounds. But "even those that don't communicate with sound are still listening to their environment," Popper says. They use sound to identify predators, for example, or suitable habitat.
A noisier world could therefore have "potentially dire consequences" for fish, warned the authors of a 2018 meta-analysis, published in Global Change Biology, which examined 42 pertinent studies. Biologist Kieran Cox of the University of Victoria in Canada and co-authors found that noise can hurt fishes' ability to find food, increase their risk of being eaten, and reduce their reproductive success.
Just how well many fish can hear in the first place is uncertain. "What we don't know is so gigantic," Popper says. Studying fish behavior in the ocean over long periods is challenging. But laboratory studies have their own limitations, Popper points out: Aquariums can change how sound waves travel, and confined fish may not behave as they would in the wild.
Scientists do know that fish are vulnerable to loud events. Popper's laboratory, for example, used a large contraption to mimic the sounds created by a pile being hammered into the sea floor. The researchers found that as the pounding sound passes through a fish's body, the swim bladder can knock into other tissues hard enough to cause serious injuries. In the wild, fish deaths have been observed near areas of pile driving. Fish in the open ocean can often flee far from loud noises, Popper notes, but those in more constrained freshwater lakes and rivers likely can't escape the din.
The belly of a male three-spined stickleback, normally dull in color but stained red-orange for the breeding season, blushes even more deeply as he swims toward a female. He faces her and repeats a zigzagging dance, darting left and right. If he's lucky, the female follows him to his nest in the sand and lays her eggs.
"They're quite cute when they perform their courtship behavior!" says ecologist Ulrika Candolin of the University of Helsinki. Sticklebacks are widespread in the ocean and in lakes; the population she studies lives in the slightly salty Baltic Sea. In recent years, she says, nitrogen and phosphorus pollution has fertilized algal blooms so severe that, on warm days, they turn the Baltic's water green.
In waters thick with algae, both laboratory and field studies have shown that romance-minded sticklebacks "have more difficulties detecting each other," Candolin says. When a pair does connect, the male spends longer than usual performing his display. And the female spends more time inspecting the male, as though unsure of what she's seeing.
Such visual interference can harm sexual selection, Candolin and colleagues found. Stickleback mating becomes more random in murky water, with females having a greater chance of selecting a less fit male, they reported in a 2016 Ecology paper. The consequences include having fewer surviving offspring. (Candolin notes that smell might also be a factor in poor mate choices—the algal blooms may obscure scent information that female sticklebacks would normally use to judge males.)
So far, Candolin notes, the sloppier mating caused by murky waters isn't hurting stickleback populations in the Baltic. Their numbers are actually growing; a decline in predators, also due to ecosystem changes, might be a factor. But Candolin's work has helped highlight how visual pollution might take a toll in the future. "Females are wasting their time and energy" when they select suboptimal mates, says Grant Brown, an ecologist at Concordia University in Montreal, Canada, who says Candolin's work on mate choice is "very nicely done."
Another risk of not clearly seeing your partner is that you will mate with the wrong species. Africa's Lake Victoria, for example, hosts hundreds of species of fish called cichlids. Females choose mates on the basis of their distinctive bright colors. But the number of cichlid species has declined, researchers found in the 1990s. Meanwhile, runoff from deforestation and agriculture has fertilized and clouded the lake waters, causing females to struggle to recognize males from their own species. They seem to end up mating with other species, resulting in hybrid offspring that sport duller hues. Not only could hybridization take a toll on species diversity, Brown says, but the mismatched mates may produce offspring that can't compete or reproduce, harming populations.
Polluted water may obscure other crucial signals. Brown, for example, has found in the lab that chemical pollutants appear to mask important molecules that fish use to sniff out danger. Fish release those molecules in their urine when disturbed; the odors warn other fish that a predator may be nearby. But high levels of nitrogenous pollutants, such as fertilizer runoff in streams, can overpower the warning scents. Brown says detecting the signal becomes "like trying to hear someone in a very crowded room with lots and lots of background noise."
Pollution can also chemically alter a different warning signal, he found: molecules that leak from fish skin when damaged, for example, by a predator's attack. Freshwater acidification, caused not by rising CO2 levels, but by airborne sulfate and nitrate pollution, may render those molecules unrecognizable. To better understand the possible consequences, Brown and co-author Chris Elvidge, now of Carleton University in Ottawa, used meter-long threads to tether baby Atlantic salmon to stream bottoms. Normally, the young fish would respond to the smell of other fishes' alarm cues by dropping to shelter in the gravel. But when the researchers returned 6 hours later, the fish in more acidic streams, which were less able to detect those cues, were likelier to have vanished, apparently because they didn't duck from danger. Sometimes a full-bellied trout had taken the place of the young salmon on the end of the thread.
Researchers are not only documenting how sensory smog harms fish, but also searching for ways to protect them from it. Some marine reserves, for example, already ban certain activities, such as construction or exploration for oil. But as researchers learn more about aquatic soundscapes, they can imagine other ways of protecting fish from unwanted sound, such as by barring loud motors or industrial activities from key fish spawning grounds during certain seasons.
Larger global issues, such as ocean acidification and polluted runoff, could be harder to tackle. Even here, however, "There are rays of hope," Brown says. For instance, he found that fish can associate a given smell not only with risk, but with a certain habitat or time of day. If a predator hunts only at dawn or dusk, the prey fish may learn to ignore the smell of that predator at midday. In a world where some of their sensory cues are masked or changed, fish may find new cues and learn new rules to live by.
Fish may also be able to cope with some interference because they have multiple ways of sensing the world. For example, fish have lateral lines, a set of organs on the outside of the body that sense pressure and currents and help fish orient themselves. Some species can also sense magnetic fields. Sharks and their relatives can detect electricity. "In some cases, if one sense is blocked or unusable, then fish will just switch to another one," Kelley says. "That makes them very resilient in that context."
The rapid pace of environmental change, however, is testing the sensory resilience of fish as never before. The outcome of rising sensory smog "could be not as bad as we're anticipating," Dixson says. "Or it could be 1000 times worse."