CHAPTER NINE

Fish symphonies

On the fringes of the Gulf Stream, off the east coast of Florida, the sea is very deep and very blue. I hold tight to the railing on the fly deck of the dive boat that rolls sharply from side to side, and look down into water that’s a thicker, denser colour than I’ve ever seen. For a moment I imagine that if I leaned over the side and dipped my hand in the water it would come out coated in blue, like paint. Golden fragments of seaweed float by, escapees perhaps from the Sargasso Sea’s swirling gyre. I would have been content to stay on deck, watching the sea’s colours go by, but there are deeper things for me to see. I pull on my dive gear and jump in. Beneath the waterline, as I kick downwards, the colours lose their intensity and slowly fade away.

Sitting on the sandy seabed at 30m (100ft) is a shipwreck. It’s a tanker that was seized in 1989 after US customs found it stuffed with marijuana, and was then deliberately scuttled and sunk to create a new underwater habitat. I aim for the deck that’s become fuzzy with a halo of seaweeds, corals and other soft creatures, and hunker down behind the gunwale in a quiet spot away from the current.

Dark shadows lurk nearby, in a hatch in the tanker’s superstructure. Before I see the animals inside I hear them, or rather I feel them push pressure pulses into the water that resonate through my body. The bass notes are probably around 50 or 60 hertz, the lower notes on a pipe organ. Another boom and I notice the wreck is vibrating. Then a fish reveals itself, a Goliath Grouper. Its looks as if it was carved from a great chunk of granite; it may well weigh as much as a Grizzly Bear.

Since the wreck was installed on the seabed, the Goliaths have adopted it as a seasonal home where they congregate in the summer months to mate. There are, though, far fewer of these fish across the mid-west Atlantic than there once were. Not so long ago, their meat was canned for dog food, and their carcasses used to smuggle drugs into the US. For decades they’ve been a favourite of sports fishermen who love to reel them in, hold them up for photos, then throw them back into the sea, already dead. A 2009 study measured the Goliath Grouper’s historic decline using archives of trophy photographs taken by sports fishermen; in the 1950s, the catch of Goliaths often outweighed the human passengers on board a sport fishing boat, but their numbers had already been decimated by the late 70s.

Following prohibition on hunting them in US waters in the 1990s, Goliaths seem to be doing a little better, at least in east Florida.1 If you venture underwater at the right time of year, there’s a good chance you’ll find a crowd of these giants and hear the deepest fish voices in all the oceans. It’s not clear exactly what meaning lies behind these sonorous calls – a warning, perhaps, or a male showing off to females – but there’s little doubt that these big fish are indeed talking to each other.

It would be easy to assume that fish are silent and unhearing creatures. They don’t have ears, at least not ones that stick out of their heads. And the sounds of the sea stay trapped below. Most sound waves don’t pierce the waterline but bounce back down into the depths. Fish certainly do make and hear sounds, but it’s taken a long time for people to realise just how sonic their aquatic world can be, partly because we ourselves are not well adapted to hearing when our ears are full of water. Normally, airborne sound waves travel down a canal towards our inner ears, making our ear drums vibrate, but when that canal is flooded it dampens the quivering membranes, muffling the sound.

The handful of noisy fish that have been known since antiquity are ones that protest loudly when they’re taken out of water and dangled in fresh air. Aristotle wrote about fish that call like cuckoos, grunt or make piping sounds; there were also, he said, some sharks that squeak.

Another difficulty in hearing fish sounds underwater is the fact that normally, in air, the slight delay between sound waves reaching our left and right ears tells our brains where the sound is coming from. Travelling so much faster in water, sound waves hit both ears almost simultaneously, making it hard to pinpoint the source. In between my noisy breaths when I’m scuba-diving, there’s often a diffuse cloud of sound all around me. It takes something as loud and obvious as a booming Goliath Grouper to give me a good idea of what’s going on.

All in all, human ears are not good at picking up and distinguishing the sounds of fish. To make sense of underwater noise, to fully appreciate how talkative fish can be, we need special recording devices to do the listening for us, and it wasn’t so long ago that those came along.

In December 1963, a woman with short curly hair sat behind the wheel of a grey Chevrolet sports wagon as she drove north from Rhode Island, along America’s eastern seaboard towards Maine. The car was packed with gadgets; there were banks of waterproof microphones, spools of cables hundreds of metres long, two-way radios and walkie-talkies, battery packs and generators, a collapsible aquarium tank made of canvas, and an aluminium boat strapped to the roof. This was a fast-response mobile listening station, on a mission to find noisy fish. The driver’s name, it just so happened, was Dr Marie Poland Fish. She was usually known as Bobbie.

As director of a research lab at the University of Rhode Island, Bobbie’s work was funded by the US Navy. Back then, the military was keen to know what sounds fish make. Historically, mariners have reported eerie sounds at sea. Moans, thumps and clanking of chains made many think their ships were haunted. This clamour became a major problem in World War II, when the hydrophones of underwater listening stations could no longer detect the distant whir of ship and submarine propellers. Submariners described all sorts of unidentifiable noises: mild beeping and fat-frying, croaking and hammering, whistling and mewing, coal rolling down a metal chute and the tapping of a stick being dragged along a picket fence. At times the racket even drowned out the biggest battleships, disabling an important part of wartime surveillance.

Following some initial investigations, it became clear that some of the noise came down to waves, wind and tides, but animals were chiefly to blame. Fish were so noisy they triggered underwater bombs, which were only supposed to detonate at the sounds and vibrations of a nearby submarine. There was obvious strategic advantage to be gained from knowing more about the hubbub of sea life, including when and where it was noisiest, which is where Bobbie Fish came in.

When the war finished, and for the next 20 years, she set out to record and identify these unseen sound-makers, most of them fish. Using hydrophones developed as part of the war effort, she fixed long-term listening stations in rivers and bays to gather ambient sounds of the underwater world. Between 1959 and 1967, a research boat went out every week into Narragansett Bay, off the coast of Rhode Island, and brought back fish to Bobbie’s lab, where she recorded their voices. With hydrophones dangling in the tank, captive fish were recorded at different times of day and in different circumstances: when they were new to the tank, when other fish were added and things got more crowded and boisterous. For the fish that stayed stubbornly quiet Bobbie administered a mild electric shock, which often elicited a prolonged audible response. Experts have criticised this approach, because it’s possible some of those sounds may not have been natural noises the fish would make without being zapped.

The team also auditioned fish in other research labs and aquaria in America and the Caribbean, and they hit the road in Bobbie’s customised car. On that December trip, the car’s first excursion, Bobbie was heading for Boothbay Harbour in Maine to record a chorus of winter fish. With her were oceanographer Paul Perkins and electrical engineer William Mowbray, whose voices you can hear on the archived recordings, announcing the name of each fish.

In 1970 she co-wrote with Mowbray Sounds of Western North Atlantic Fishes, a book filled with spectrograms, showing the shape and texture of fish sounds.2 The mix of tones and pitches in a fish’s voice were plotted in charts, revealing the intricate differences between croaks and barks, hums and grunts. The book contains spectrograms from the fish Bobbie recorded in Boothbay Harbour, like the Pollock that was lowered into the canvas tank and made thumping sounds when it was handled; its spectrogram shows repeated smears of sound, like a comb dragged through paint. Another Boothbay fish from 1963 was the Grubby, a type of sculpin, whose spectrogram has two clean lines, one lower- and one higher-pitched, both lasting for four seconds, then again for two. The book also features the voice of an Ocean Sunfish that was found just outside Narragansett Bay and held in a sea pen; it made rasping grunts like a pig, which became louder and more frequent the more it was handled. A Goliath Grouper in Puerto Rico let off a tremendous boom whenever it was prodded, producing a spectrogram that looks like a series of short strokes of a soft paintbrush; another in the Bahamas stayed quiet, although it did, on one occasion, almost swallow the hydrophone in its enormous mouth.

These findings helped navy personnel to tune out the sounds of fish and once more tune into the sounds of their enemies. Bobbie Fish had used her listening devices and analytical tools to pick out individual voices from the underwater cacophony. She had shown that it’s not just a few fish species that are noisy, but hundreds of them. And as she wrote in the introduction to Sounds of Western North Atlantic Fishes, ‘The mechanisms for sound production in fish are varied and often ingenious.’

Just like their abilities to make electricity and toxins and light, fish have evolved ways of making sounds many times. They’ve transformed different parts of their bodies into noise-making instruments. Fish gnash their teeth to make rasping sounds; anemone fish have tendons that snap their jaws shut and their chattering teeth make chirps and pops; coral reef-dwellers called grunts get their name from the grunting sounds they make by grinding their second set of teeth together, at the back of their throats (their pharyngeal teeth); porcupinefish rub their toothless jaw bones together, making a sound like a rusty hinge. Seahorses click when they flick their head upwards to catch plankton and two bones at the back of their skull push past each other; they also purr and growl, sounds generated somehow in their cheeks (with a mechanism that isn’t yet fully understood). Sculpins use muscles to rattle their pectoral girdle.3 Channel Catfish, a common sight and sound in North American rivers and lakes, rub serrated fin-spines over a roughened patch on another bone, in a similar way to how crickets and grasshoppers sing and chirp. Croaking Gouramis are popular pets and native to still waters of Southeast Asia, in ponds and paddy fields; their croaking name comes from the sounds they make when they beat their pectoral fins against specialised tendons, like strumming a guitar.

The most common body part that fish use to make sounds is their swim bladder. This internal gas balloon – commonly sausage-shaped or like a modelling balloon that’s been twisted part-way down into two lobes – first evolved in fish as a lung to breathe through, then was co-opted as a flotation device, and later adapted in many ways to emit sounds.

Think of all the different sounds you can make with a regular balloon. You can drum your fingers against it, make it squeak by rubbing its surface against something else, or you can let a trickle of air out in a squeaky whine; fish do all these things and many more. The only thing they don’t do (on purpose) is pop their swim bladders to make a loud bang.

Many fish have sonic muscles that vibrate against the swim bladder, making it buzz and hum as it contracts and expands. Some have muscles that stretch the swim bladder forwards then let it go, so it pings back into place. Triggerfish have a drum on each side of their body where the swim bladder pushes up against a patch of large scales called scutes. Struck by the pectoral fins, the scutes bend inwards, then pop back into shape, making a drumming sound. Toadfish, some of the noisiest of all the fish, call out like a foghorn by rapidly vibrating their heart-shaped swim bladders. Two sets of sonic muscles make each portion of the toadfish’s bladder buzz at different rates, producing complex sounds similar to the wailing cries of a human baby, sounds that are hard to ignore (especially if you are a female Toadfish).4

Learning precisely why fish make sounds and what uses they serve involves not just listening to fish but also watching them. Film footage reveals that many species use sounds as alarm calls, shouting aggressively when picking fights and screaming to startle predators. Amazonian Red Bellied Piranhas yell at each other with a certain level of sophistication, using three distinct calls in different circumstances. During head-to-head encounters before a fight breaks out, the fish emit sharp repetitive barks as a warning of what lies in store if their opponent doesn’t back off; it’s a piranha version of trash-talk. Then, when a skirmish breaks out, especially competing over food, the piranhas make a deeper thudding sound while they circle aggressively and take bites out of one another. Both of these hostile noises are made by muscles vibrating the swim bladder. A third call is a volley of much higher-pitched sounds, made by gnashing their teeth. When a victorious piranha chases off another, it makes this sound, presumably to say, ‘I win. You lose. Don’t come back.’

Pacific and Atlantic Herring are far less furious fish. They seem to communicate with gentle streams of bubbles trickling from their swim bladder and out through their anus. Emanating from the trails of bubbles come pulses of sound, up to seven seconds long, which researchers named Fast Repetitive Ticks or FRTs for short. Film footage shot in huge aquarium tanks in the dark with infrared cameras shows young herring swimming around in loose shoals, making bubbles. With a screen across the top, blocking their access to the air, the herring quieten down after a few nights, probably because they can’t refill their swim bladders by gulping air from the surface into their stomachs, and they run out of farts.5 One idea is that they use bubbles to maintain contact with their shoal-mates at night. When the lights come on and they can see each other again, the herring fall silent. They’re the only animals known to communicate with flatulence.

Often, the rowdiest periods underwater are when fish are courting and mating. Deep beneath the springtime waves of the North Atlantic, male Haddock swim close to the seabed in tight circles and figures of eight, and they emit slow repeated knocks (they will also perform their mating rituals in large aquarium tanks, which is how we know they do this). The noises are important because it’s dark and murky down there. Females hear the calling males and come to investigate. A male will then trail after a female. He’ll also swim ahead and get in her way, flicking his fins at her and showing the three spots he’s drawn across his flank, by shifting pigments around inside the chromatophore cells in his skin; normally there’s just one dark mark, his ‘Devil’s Thumbprint’, as it was traditionally called. All the while he speeds up the pace of his knocking. He begins to sound like the roaring engine of a motorbike as the knocks blend together into a constant, loud hum. For at least ten or twenty minutes he can hum non-stop. Eventually, if he’s lucky, the female swims upwards and they press their bodies together into a tight clinch. The male’s voice reaches a quavering finale as he releases a cloud of sperm and, perhaps signalled by his climactic cry, the female puts thousands of eggs into the water. Then the male falls silent, and the pair break apart and swim off. This is what Haddock are usually up to when they’re scooped from the sea by North Atlantic trawlers that target their spawning sites.

Humans also have their own mating rituals involving fish swim bladders. A century or so ago in Europe, they were fashioned into reusable condoms. Catfish and sturgeon swim bladders were, apparently, a popular size and they needed to be tied in place with a ribbon. In China, soup made from dried swim bladder is considered an arousing delicacy. One species in particular, giant croakers called Totoaba, live only in the Sea of Cortez, and have a sky-high price ticket on their swim bladders (or maws). The illegal trade is taking so many fish they’re now critically endangered, as is the world’s smallest dolphin, the Vaquita, another endemic to this small sea in Mexico. Vaquita get tangled and drowned in the gill nets set to catch the valuable Totoaba. It might not be long before both species go extinct, and all because of soup.6 There are people who pay a lot of money to slurp a bowl laced with Totoaba maw, believing it boosts fertility and contains potent aphrodisiac powers.

Fish swim bladders are still used today to clarify beer. Rich in the protein collagen, dried swim bladder speeds up the rate that yeast clumps together, so it settles out of beer quickly, leaving it sparkly and clear. British breweries originally used sturgeon swim bladders imported from Russia, a by-product of the caviar industry. With rising prices an alternative was sought and in 1795 Scottish inventor William Murdoch showed that much cheaper swim bladders from Atlantic Cod work just as well. By the 19th century, pale ales became popular instead of dark porters and stouts, as pub-goers quaffed transparent pints in see-through glasses rather than china and metal tankards. Lately, there’s been a backlash against using swim bladders, also known as isinglass, and more breweries are using vegan-friendly alternatives like seaweed, or they’re learning to be patient and wait longer for yeast to settle by itself (or they’re simply persuading customers to accept cloudy pints).

A whiff of magic surrounds another piece of the fish’s sonic equipment. For a long time, people have been rather obsessed with the mystical and curative powers of stones allegedly found inside animals, including snakestones and toadstones,7 and fish are no exception. Lodged deep inside fish heads are small, hard stones known as otoliths (from Greek words oto and lithos, meaning ‘ear’ and ‘stone’). In the first century, Pliny the Elder wrote about these stones being used as charms against swellings in the groin and pains in the eye. Sixteenth- and seventeenth-century literature refers to them being ground up, mixed in wine and used to treat kidney stones or nose bleeds; you can wear one as an amulet to ward off malaria. And naturally, as with so many animal potions, it was said that fish stones could enhance the libido. In his 1502 book Mirror of Stones, Italian astronomer and mineralogist Camillus Leonardus wrote of magicians who professed that otoliths ‘excited Luxury in the Day’ – in other words, they can lead to amorous behaviour, for some reason before the sun sets.

Today, otoliths continue to be widely treasured and put to many uses. Fishing communities in Iceland, Brazil and Turkey still use ground otoliths in folk remedies to treat urinary infections and asthma. Spanish fishermen keep otoliths in their pockets to protect them from storms at sea. And in North America, beach combers on the shores of Lake Erie may come across otoliths that came from a Sheephead, a species of croaker. These fish have pairs of otoliths that form a mirror image of each other, one from each side of their head. Some have a J-shaped groove running across them and, supposedly, bringing joy. Otoliths impressed with the letter L are known as lucky stones and will bring good luck, or perhaps even love.

There’s no evidence that otoliths hold any real healing or lucky power for humans, but for fish they play an important role in hearing. Because fish swim in water that’s a similar density to their bodies, sound waves tend to pass straight through them. To make up for this they have large granules inside their inner ears made of calcium carbonate, the same material that seashells are made of. Otoliths are denser than water and the rest of the fish’s body, and they move more slowly in response to a sound wave, rather like the white plastic flakes inside a snow globe when you shake it. The structure of a fish’s inner ear is similar to our own. They have fluid-filled chambers, similar to the human cochlea, lined with sensory hairs. Inside each chamber is an otolith.8 As the otoliths vibrate against the sensory hairs they trigger nerve signals to the brain. Also, as the otoliths sink down under gravity, they tell the fish which way is up; flying fish have especially big otoliths, perhaps because their sense of balance is so important while they glide through the air.

If all you have is a fish’s ear-stone, there’s still a lot you can know about the animal it came from. Similar to molluscs making their external shells, fish continually lay down new layers of calcium carbonate inside their ears. With the aid of a microscope, you can count the layers and know how old a fish was when it died. With a lot of patience you can distinguish the protein matrix sandwiched between daily layers of calcium carbonate, and work out how many days the fish lived for. You can identify a fish species from its ear-stones: some look like sea-smoothed chips of beach glass, and others like jagged rice puffs. The outer edge of an otolith can look a little like waves on the surface of the sea, which might explain another long-standing belief that a fish’s head-stones can forecast conditions at sea. In reality, otoliths can’t predict the future, but they can tell us about the past.

There’s a chemical story written into every fish’s ear-stone that records details of its life. As they grow, otoliths pick up minute traces of other elements from the water, like barium and magnesium, and the amounts vary from place to place in oceans and rivers. By measuring these chemicals locked up in otoliths, it’s possible to work out what the fish ate and where it swam at different times of its life (like the giant Amazonian catfish), even the temperature of the water. And the fish doesn’t need to have died recently. Otoliths are so dense and tough they commonly hang around long after the rest of the fish has rotted away, and they fossilise well. Palaeontologists have extracted the stories of fish from otoliths that fossilised hundreds of millions of years ago, and used them to work out the temperature of ancient oceans.

As well as their ears, fish have an entirely separate series of sensory organs laced across their heads and flanks. Known as the lateral line, this effectively converts their whole body into a giant ear. It’s an ancient structure that evolved very early on; the oldest known fossilised lateral lines are in jawless fish from the Ordovician period (around 480 million years ago) and all living fish groups have them.9

The basic units of the system are structures known as neuromasts, which that contain tiny hairs that fire nerves when they bend, working in essentially in the same way as hairs in the inner ear. Neuromasts can either sit on the skin surface or lie inside tubes that run under a fish’s skin and scales. Lines of dots along a fish’s flank shows the points where water enters these tubes. The system lets fish sense the flow of water over their body and detect vibrations close by, at one or two body lengths away. Hunting fish pinpoint the noisy vibrations of insects that fall into the water and kick and struggle on the surface. They also track ghostly imprints that other animals leave behind as they push their way through the water. After a creature passes by, it sheds a wake that lingers for some time. And by the quivering of its lateral line, a fish can know the size and speed, and even the particular swimming stroke of that animal, and decide whether to follow in pursuit or make a quick escape.

Lateral lines are especially important for fish that live in the dark and have no eyes, such as Mexican Tetras. Like other, seeing fish, they use their lateral lines to locate moving objects that swish past. Blind fish can also detect stationary objects, like the walls of their cave, by sucking water into their mouths and sensing any pressure disturbances in the flow that tells them when they’re about to bump into something. The closer they get to an object, the faster they open and close their mouth, presumably to create a faster flow and gain more information about what’s out there. Bats flying through these underground caves use ultrasonic beams to hunt and navigate, while down below fish interrogate the cave’s waterways with their equivalent of echolocation.

The fish that hear the best are the ones that don’t rely solely on otoliths or the lateral line, but have a helping hand from their swim bladders. These compressible balloons of gas not only make sounds but detect them too, by vibrating when the pressure waves of sounds pass through. It’s another big secret behind the immense success of fish: thousands of species have modified their swim bladders into listening devices.

One way they do this involves a chain of jiggling bones, adapted from four or five vertebrae of the neck, that connects the swim bladder to the inner ear.10 These important little bones boost the hearing of one in four fish species, and they’re thought to be a key feature underpinning the immense success of the fish that dominate freshwater ecosystems – the minnows, catfish, carp, loaches, knifefish and piranhas.11 Inland waters are often murky and difficult to see through, so sound and hearing play a crucial role in the lives of many freshwater fish species.

Other fish have extensions of their swim bladders that connect to their lateral line, or poke through the skull and connect directly to the inner ear. Herring, menhaden, sardines, shad and anchovies all hear this way, and among them are the champions in high-pitched hearing.

Blueback Herring and American Shad swimming in silvery schools off North America’s eastern seaboard, and Gulf Menhaden in the Gulf of Mexico, can all hear higher-pitched sounds than any other fish. Captive specimens have been trained with weak electric shocks to lower their heart rate when they hear sounds. This revealed they can detect frequencies up to 180kHz (an average human hears between 20Hz and 20kHz), making them one of only a handful of animals that are known to hear ultrasound, along with bats and cetaceans.

A less invasive fish-hearing test involves placing surface electrodes on their skin to record the firing of auditory nerves when different sounds are played through underwater speakers (this Auditory Brainstem Response, or ABR, is used to test hearing in young human children, although usually not when they’re underwater). Wired up in this way, Goldfish have shown they can hear up to 4kHz, the highest key on a standard piano, as can most fish with swim-bladder-to-ear connections; unconnected fish can only hear up to around 1kHz.

All these tests, on herring, shad, Goldfish and many other fish, pose the same question: what are these fish listening to?

The herring and shad don’t make ultra high-pitched sounds, so at these higher registers they can’t be listening to each other. Their discerning hearing may in fact have evolved because it lets them eavesdrop on dolphins when they use beams of ultrasound to find prey, including these schooling fish. There are moths that do the same, listening out for bat sonar to avoid getting eaten. Studies suggest that herring and shad can hear dolphins from at least 100m (330ft) away. Likewise, Goldfish aren’t listening to each other because they themselves, as far as we know, are silent. They too may be listening out for the sounds of predators, or they could be listening to the assorted soundscapes of their underwater world.

When Bobbie Fish set about recording and analysing the sounds of fish, her main aim was to tease apart the cacophony of underwater noise, to identify voices and assign them to certain species. Since then biologists have, for the most part, continued to focus on the sounds that individual fish make and hear. Gradually, though, a new approach is emerging, as more people are beginning to listen to the entire aquatic symphony.

The world is bathed in light from the sun, and it’s also bathed in sound. Underwater, this soundscape may at first seem like a disorderly din, but there’s more to it than that. Off the coast of Western Australia, a series of waterproof microphones have recorded distinct dawn and dusk choruses, lasting for hours at a time. These were the sounds of thousands of fish, calling to each other, fighting, flirting, mating and eating at those most active times of day. There is structure in this noisy world.

In the cool, fish-rich rocky reefs off New Zealand’s North Island, another set of listening devices revealed that different habitats have their own particular sounds and a unique acoustic signature. By listening, it’s possible to tell apart a rocky reef covered in seaweed from one inhabited by sea urchins; as they graze and scrape the rocks with their teeth, the urchins’ shells resonate like bells.

Much remains unknown about how fish listen to these ambient sounds. It could be that they try to tune it out so they can hear each other, like having a conversation at a loud party. But there are clues that the backdrop of noise matters to them, that fish listen in and extract useful information from the sonic miscellany.

Nocturnal sounds may be especially important. In shallow tropical seas, many fish are on the move between day and night. During the day, some hide and rest in patches of coral reef or among mangrove tree roots, then as night falls they swim to nearby seagrass meadows to feed. Most make their move when it’s dark in the hope they’ll go unseen by the most dangerous predators, the bigger fish that hunt by sight. Similarly, newborn fish spend their first days and weeks in open water, again to avoid the reef’s many hungry mouths. In time, the young ones’ muscles and fins become strong enough to push against tides and currents. Only then do they turn around and begin a long swim back home, guided at night by an inbuilt magnetic compass and during the day by a celestial compass, pinpointing the position of the tropical sun beaming down on the water. As they get closer, the young fish zero in on their native habitat, following their noses and also their ears, listening for the sounds that could act as beacons guiding the travelling fish through the dark.

To investigate this idea, Craig Radford from the University of Auckland in New Zealand led a research team who built small, identical piles of coral rubble, spaced out across shallow waters around Lizard Island on Australia’s Great Barrier Reef. Through underwater speakers suspended over each rubble pile they played back soundtracks recorded in different habitats. The morning after a noisy night, Radford and his team counted up the young fish that had arrived on each rubble pile and found that some did indeed seem to be lured by the sounds of certain habitats. Young damselfish headed for rubble piles that sounded like a fringing reef (dominated by the popping and cracking of pistol shrimp as they snapped their claws) and young bream were drawn to the piles that sounded like an open lagoon; far fewer fish were enticed by the sound of silence, played back to them in the control rubble piles. It’s still early days, but it seems likely that fish can distinguish between the sounds of different places underwater, and follow their ears to the spot they most want to be.

These habitat soundscapes are subtly composed. Recent studies are revealing that far from this being an impromptu free-for-all, fish don’t simply yell and shout however and whenever they want: they fit their voices together like an orchestra of instruments in a melodic musical score.

One such study took place off the KwaZulu Natal coast of South Africa, in the Indian Ocean, a short way south of the Mozambique border. Just offshore, steep canyons carve into the seabed. A hundred metres (330ft) down, in a cave where coelacanths live, a team of European researchers led by Laëtitia Ruppé wedged a small recording device into a crevice in the wall. After two months, the team fetched the device and listened to the sounds of the cave-dwellers. Previously, South African biologists inside mini-submarines had visited caves in the area and seen hundreds of fish species living down there, including sound-making groupers, soldierfish and toadfish.12 So it was perhaps no surprise when the cave recordings played back thousands of noises, many of them fish voices. What was surprising was the patterns those voices made.

Taking the most obvious voices and plotting them on spectrograms like the ones in Bobbie Fish’s book, Ruppé’s team found that, at night, fish were acoustically avoiding each other. In two dimensions, of pitch and time, each voice occupied its own space on the spectrograph, like pieces of a sonic jigsaw; different fish called at different times or different pitches, building up distinct layers of sound. There were deep, isolated booms, low and long tones and clear, coarse pulses, pops, grunts and high-pitched whistles. The species awake during the day produced more jumbled sounds, perhaps because they could see each other and combine their calls with gestures; when they call, they can swim and flick their fins in eye-catching ways, like shouting to a friend on the other side of a busy room and waving at the same time to catch their attention. In the dark of night, when fish can’t see each other, it matters more if they have overlapping, clashing calls. Nocturnal species make sure their voices don’t drown each other out.

These fish are partitioning sound in the same way they divide up many other aspects of their ecosystem. Within a community, species evolve to eat different foods and they split up the physical space they occupy; now it’s becoming clear that species also set out and establish their own vocal territories.

The ecology of sound is still a relatively new idea, and so far has mostly been applied to terrestrial ecosystems. There are various birds, insects and frogs that similarly divide up their soundscapes and avoid masking each other’s calls. Studies on land also point to the problems that unfold for these vocal species when the world becomes noisier with human sounds. Traffic makes it difficult for birds to hear each other and they can miss important messages, particularly during mating times. It’s too early to say whether fish will suffer as we fill up the oceans with our human sounds, from shipping traffic, seismic surveys, underwater sonar and thousands of offshore oil and gas platforms. Marine mammals are the focus of most investigations into underwater noise pollution. Fish studies are few and far between. But the chances are there are many fish out there whose lives are shaped by sound, fish that are doing their best to talk and make themselves heard in the clamour of an increasingly noisy world.

 

The fish and the golden shoe

China, T’ang dynasty, ninth century

A girl called Sheh Hsien lived in a little house in the mountains with her cruel stepmother and stepsisters. They would send Sheh Hsien to gather wood from dangerous, faraway forests and to carry water from the deepest wells. One day, she pulled up her bucket and saw inside a small, shining Goldfish. It had red fins and golden eyes, and was as long as her finger. She took the Goldfish home and put it in a basin of water, where it swam round and round in circles. She fed it scraps of food and every day the Goldfish grew bigger, so she had to find larger and larger basins to keep it in. Eventually she didn’t have a vessel big enough, so she took the Goldfish outside and let it go in the pond behind her house. Whenever she came to feed it, the Goldfish would swim over and rest its head on the side of the pond. But it only came to Sheh Hsien, and no one else.

When the stepmother saw this big, fine Goldfish she was jealous and wanted it for herself. So she sent Sheh Hsien to fetch water from a well far away, then dressed in her stepdaughter’s cloak and went to the pond. The Goldfish came to the stepmother, and straight away she killed it with a sharp knife. She cooked the enormous fish over a great fire. ‘That was the most delicious fish I have ever eaten,’ she thought to herself, as she buried the Goldfish’s bones in a pile of dung.

When Sheh Hsien came back from the well and saw her Goldfish was gone, she sat down and wept. Just then, an old man wandered past who reminded her of her dead father. ‘The fish’s bones are in that dung pile,’ the old man said. ‘Go and find them and place them under your pillow. Then, if you ever want for anything at all, ask the fish and your wish will come true.’

The old man bade her farewell, and Sheh Hsien did as he said. With the bones under her pillow she began to ask the Goldfish for many things and soon she had beautiful clothes and shoes, jewellery and pearls, and the finest food to eat. She missed the Goldfish, and hated her stepmother more for than ever for stealing and eating it, but she was thankful for everything it was now bringing her.

A while later it was the Festival of the Mountain, but the stepmother forbade Sheh Hsien from going. When everyone had left the house, Sheh Hsien dressed herself in a blue silk dress and golden shoes, and sneaked out to join the party. She hadn’t been there long when one of her stepsisters spied her and Sheh Hsien ran away. As she fled she tripped and one of her golden shoes fell off.

A crow picked up the glittering shoe, then flew off across a great sea and dropped it on an island that belonged to a powerful king. When the king saw the delicate shoe he ordered his men to find its owner. All the island’s women tried on the shoe, but their feet were too big. The king sent his men to search houses far and wide, until they came to Sheh Hsien’s house on the mountain and found a single, matching golden shoe. She slipped her feet into both tiny shoes and the king fell instantly in love with her. After that, the king and Sheh Hsien were married and lived happily together on his island, and Sheh Hsien always remembered her lucky Goldfish.

Notes

1 At the time of writing there are calls to allow fishing of Goliath Groupers once more, despite scientists’ warnings that this will once again deplete the spawning population.

2 Spectrograms plot sound wave frequency on the y axis against time on the x axis; the higher the frequency of the sound wave, the higher the pitch.

3 The pectoral girdle in humans is made up of the shoulder blade and collar bone.

4 These are known as non-linear sounds. Filmmakers make use of the way these sounds heighten an audience’s emotional response by adding them to sound tracks at key moments; Alfred Hitchcock used them in the shower scene in Psycho.

5 Herring and other so-called physostomous fish (including birchirs, gars, some catfish, eels and trout) have a pneumatic duct between the gut and the swim bladder, allowing them to fill up, fart or burp out gas from the bladder. Other fish, the physoclisti, have lost that connection and instead have a gas gland that pumps gas more slowly in and out of the swim bladder.

6 At the time of writing, there are estimated to be fewer than 30 Vaquita alive, and efforts to breed them in captivity have recently failed.

7 Which were nothing to do with toads but were in fact the fossilised teeth of extinct Lepidotes fish.

8 Ray-finned fish have six otoliths; lampreys have four, hagfish have two. Sharks’ otoliths are the size of sand grains.

9 The only other animals that have an equivalent system are amphibians, and mostly just in the larvae.

10 These bones, known as the Weberian apparatus, do a similar thing in as the incus, malleus and stapes in our own ears, which transmit sound waves from the eardrum to the inner ear.

11 These and many other fish belong to a group known as the otophysans, which account for more than 60 per cent of all freshwater fish species.

12 It’s not clear whether coelacanths are vocal or stay quiet among their chattering neighbours.