How Fish Talk

Eric Parmentier appreciates a good fish song. He's spent the last 10 years traveling the world, planting underwater recording devices everywhere from Japan to Madagascar, and listening in on fish sounds that are as diverse as the species themselves. "I want to have a global view of communication in fish," the Belgian biologist told me.

His worldview is being shaped by the thousands of species of chatty fish in the sea, each with its own song and its own unique broadcasting anatomy. In a great example of convergent evolution, fish have assembled a number of strategies for producing sound. Some vibrate swim bladders or resonate bones, and others make use of hyper-fast muscles that contract up to 200 times a second. And now, a few scientists are even discovering that fish have developed ingenious ways of manipulating their environments in order to make their songs sound better.

Parmentier's quest recently took him halfway around the world to French Polynesia in order to track down a communicative fish that displays some unusual behavior. The ​pearlfish, in the family Carapidae, is probably best known because it likes to live inside the butts of sea cucumbers, but it can also make its home in starfish, clams and oysters. This intrusive fishy tenant racked up another accolade this December, as Parmentier and an international team of researchers ​published a paper showing that one species of pearlfish, Onuxodon fowleri, may be using its host to amplify its calls like a natural speaker, sending them farther into the deep.

Parmentier and his PhD student Loic Kever didn't set out looking for this finding, as they were more interested in the bizarre relationship between pearlfish and their unfortunate invertebrate hosts. Not only do pearlfish live inside other animals, some species even breed inside them and feed on the gonads of their lowly landlords. While there are numerous species in the pearlish family, Parmentier has never found two different species in the same host. "So there is certainly a system of identification, meaning also that ultimately sounds are used for territory defenses," he said.

How might a small fish that lives its life inside a clamshell get his message out? To understand this the team had to set up shop on a small chain of island atolls in the Pacific. After diving in the idyllic tropical location for about a week, Parmentier and Kever located a lagoon off the remote atoll of Makemo where 70 percent of the oysters contained at least one, but usually two pearlfish. They set up recording equipment in the lagoon and noticed that the fish's sounds were able to be heard as far as 40 meters away, an impressive shout out from an animal only 7 cm in length.

"Fish living inside a host with hard tissue are quite rare and we wanted to know if this kind of host impacts acoustic communication," explained Kever, Parmentier's grad student.

The team brought some specimens back to the makeshift island laboratory where they attempted to record and characterize their unique calls, but the fish would not cooperate. They would only make sounds if they were inside the oyster shells. It was then that Parmentier thought back to ​a paper written by  Italian ethologist Marco Lugli in 2012 that demonstrated rocks and shells on the sea floor were able to amplify small, low frequency sounds. That's when it dawned on Parmentier that maybe the pearlfish knew something he didn't.

Parmentier phoned Lugli back at his lab at the University of Parma with this idea. Lugli agreed it was something to pursue and had the shells shipped to his lab at the University of Parma to be tested for their resonance capability. He put them in tanks with a tiny underwater speaker placed inside the shell that beamed white noise (a collection of tones in varying frequencies) into the shell cavity in order to mimic a soniferous fish. To his surprise the shell was able to amplify the sound in three different frequency bands—an amazing finding that hints at the possibility that these little fish may have found a way to make a big sound.

Audio courtesy Marco Lugli

Jacques Cousteau had it wrong when he named the title of his epic 1954 documentary ​The Silent World, because the seas are anything but silent. First, there are the turbulent sounds of water bubbling and breaking, there are the thousands of chatty fish pulsing, chirping, growing, rattling and even hooting to communicate, not to mention gnawing and gnashing at food, and then there are the ​man-made noises associated with shipping and boating.

From an evolutionary perspective, it makes sense that if a little fish can use its environment to boost its signal over all this background, it may be able to gain a major advantage in finding a mate or perhaps defending its territory. But how can a little fish do this?

"The big thing people always wondered about for years and years with the ​toadfish, for example, was how does such a small radiator make such an impressive sound? With the toadfish, it's like you are sending a tweeter to do a woofer's job in terms of speakers," said Michael Fine, biologist and leading bioacoustics researcher at Virginia Commonwealth University.

Sound waves are simply pressure waves. This means that the louder the sound, the more energy it has and, just as a small speaker makes a smaller sound, a smaller fish should as well. But in addition to being loud, many small fish make low frequency noises, which is also puzzling. Low frequency noises have longer wavelengths and require more energy to produce, especially underwater where the speed of sound is five times greater than in air (remember high school physics here, with speed of sound = wavelength x frequency). How does a violin make a bass note?

Perhaps the animal has adapted to make due with what it has. The aforementioned toadfish can vibrate its swim bladder 200 times a second, producing a nice low frequency tone of 200 Hz. But Marco Lugli may have found another explanation.

Prior to the pearlfish work, he had been studying a small freshwater Mediterranean species of goby, Padogobius bonelli, that makes its home inside burrows in the riverbeds of northern Italy. The fish has a rather elaborate courtship ritual in which it burrows a hole into the gravel, typically underneath a rock or shell. In other species of goby, like the smaller, saltwater-dwelling Pomatoschistus minutus, the male actually piles sand on top of his shelter. In both species, the male shimmies his body around, digging out a burrow, then hunkers down in his nest, occasionally calling out to a female passerby.

If the female wants to mate, she enters the nest and lays her eggs, all the while being serenaded with the male's songs. Traditionally, biologists explained the shelter and curious sand piling effort as a means of camouflage or a way to demonstrate his desirability as a mate—but Lugli sensed there was more at play.

Like many other burrowing fish, the goby is not alone in preferring to vocalize inside a burrow or cavity—so do blennies, toadfish and darters. The setup is not unlike an organ pipe, and Lugli had the hunch that there might be an acoustic effect. He gathered shells and rocks from the streambed and recreated the goby's cavity in a laboratory tank with the same miniature speaker used on the pearlfish's oyster shells.

Lugli found that the goby-made shelters did in fact act as natural amplifiers for low frequency sounds, in some cases boosting sound levels ​as much as 18 dB in the range of 20-200 Hz—precisely in the gobies' vocal range.  And what about the saltwater goby's tendency to heap sand purposely on top of the nests? Turns out they have a nice effect on sound production, ​increasing the amplitude by another 12 dB. Perhaps the smaller the fish, the more inventive they have to be.

"Producing sound inside a cavity might help the fish to circumvent or, at least, mitigate the constraint of a small size on sound production, and might partly explain why so many small fishes (for instance, toadfishes, gobies, blennies) call inside cavities and use low frequency sounds," said Lugli about the findings.

These studies provide a remarkable example of fish that may be taking advantage of the environment to make communication more effective. Lugli's work offers the possibility that the goby's nest provides acoustic clues to its mate. There is some evidence that damselfish, for example, have ​been shown to recognize calls from members of the same species, which provides some evidence that these calls could be useful in mating.

"I think the use of shelters that amplify the sound simply gives them the bonus of a louder sound that can be heard further or may convey a more effective message to females and rival males," said Michael Fine. It has ​been shown that larger gobies make louder sounds, and one could imagine that if the female happened to prefer larger males, a small male could appear larger by constructing a nice amphitheater to play his song.

This research opens the possibility that fish are using their environment to make their voices heard, devising a range of remarkable solutions to the challenges of communicating under water. From oyster shells to goby burrows, the diversity is striking and it is what impresses Parmentier the most.

"Each time I place hydrophones I am very impressed on the number of different types of songs I can record," he said. "The most interesting part is just trying to explain the different mechanisms fish have to make sounds. The diversity is wonderful."