With the exception of the cast of Disney's The Little Mermaid—and Big Mouth Billy Bass—fish do not spring to mind as the animal kingdom's most vocally gifted members. But one unusual singing fish has been teaching biologists and neuroscientists a lot about speech and hearing. Its bulging eyes and blubbery lips have graced several research posters at the Society for Neuroscience's annual meeting, which is in New Orleans, Louisiana this year.
The finned crooner in question is the plainfin midshipman fish (Porichthys notatus), which belongs to a family of fish known as toadfish because of their squat, slimy appearance. Midshipman fish live along the Pacific coast from Alaska to Baja California at depths of up to 300 meters, burying themselves in the mud during the day and surfacing at night to feed. Their name is attributable to the hundreds of luminous spots called photophores that decorate their underbellies, which are somewhat reminiscent of the buttons on a naval officer's uniform. The fish likely use these bioluminescent dots to attract small prey such as krill and to hide from predators by masking their own shadows with a camouflage technique known as counter-illumination.
Midshipman fish come in three varieties: females, Type I males and the smaller Type II males. All three types are vocal, emitting short grunts to communicate with one another, but Type 1 males are the most voluble by far. In the spring and summer, Type 1 males head to shallow waters, excavate nests beneath rocks along the shoreline, hunker down and start to sing, using sonic muscles surrounding their inflatable swim bladders to hum for up to an hour at a time. This humming, which people have described a droning motorboat or an orchestra of mournful oboes, is so loud that it has been known to wake houseboat owners in San Francisco and Sausalito (Listen to a clip of the humming here). Female midshipman fish follow the singing to the Type 1 males' nests, where they lay their eggs. Type II males are little sneaks. They also listen for the calls of Type I males and look similar enough to females to slip past a Type 1 male and fertilize any recently laid eggs in his nest before the Type 1 male gets a chance to release enough of his own sperm.
Studying how midshipman fish call and respond to one another has taught scientists about the evolution of vocal communication and the neurobiology of hearing. In one study, Andrew Bass of Cornell University traced the development of the midshipman fish nervous system and brain, focusing on neurons that control their sonic muscles. The fundamental structure of the brain circuit he traced was remarkably similar to neural circuits in corresponding brain regions in amphibians, birds and mammals. Because toadfish first evolved so long ago, Bass concluded that this particular neural circuit is likely 400 million years old—almost as old as vertebrates themselves. Of course, different groups of animals have tinkered with this basic neural archetype over the course of evolution—and developed very different systems of muscles and tissues for vocal communication—but nonetheless our own speech and song owe a lot to the ancient grunts and hums of midshipman fish. In more recent work, Bass has continued to explore the underwater origins of vocal communication, as well as whether fish were the first animals to evolve some common non-vocal gestures.
Bass and his colleagues have also discovered that Type 1 male midshipman fish deliberately desensitize their ears to sound when they are humming to avoid damaging their ear hair cells. At the same time that a male midshipman fish's brain stimulates muscles surrounding the swim bladder, it sends electrochemical messages to ear hair cells, essentially telling them to put in earplugs. These two types of signals happen in sync about 100 times every second. Since all vertebrate brains have similar living links to the ears, Bass and his colleagues propose that four-limbed animals like echolocating bats, barking dogs and human pop stars might rely on related acoustic strategies to protect and preserve their hearing when they are making loud sounds.
Now, Elizabeth Whitchurch, currently at Humboldt State University, and her colleagues have shown that Type 1 males have bigger distances between their swim bladders and their ears than Type II males and females. This adaptation may further help Type I males protect their hearing during the mating season. Whitchurch presented her findings at the Society for Neuroscience's annual meeting.
In related research, Joseph Sisneros of the University of Washington and his colleagues have established that as the breeding season approaches, sex hormones flood the bloodstreams of midshipman fish, which in turn changes their singing and hearing. Female midshipman fish are most attuned to the males' mating calls when their estrogen levels are high. Similarly, the most successful male baritones have the highest levels of testosterone. In addition to teaching researchers how hormones modulate the nervous system, studying these changes could help scientists understand whether people's hearing declines as they get older in part because of waning hormone levels. In some studies, mice deficient in estrogen or estrogen receptors suffer faster and more severe hearing loss and scientists have proposed that hormone therapies could stave off age-related hearing loss in women.
When it comes to animal research on speech, music and hearing, songbirds like zebrafinches and squeaking mice usually get the spotlight. Who would have thought that a humble mud-dwelling toadfish would give scientists so much to say about vocal communication? In honor of this unlikely inspiration, let's make some noise: three cheers—or grunts—for the plainfin midshipman fish!