Many males across the animal kingdom sing to attract a mate: birds are arguably the most famous, right behind adolescent human males; other notable examples include frogs, humpback whales, and crickets. A fish likely didn’t even come to mind; yet, the plainfin midshipman (Porichthys notatus), an intertidal fish that inhabits the San Francisco bay, among other places in the Pacific, does in fact sing.
Just as “beauty is in the eye of the beholder” for visual signals, the loveliness of this fish’s “song” is in the ear of the listener. It truly is a melody that only a female plainfin midshipman could love; to the human ear, it sounds like nothing more than the incessant droning of a boat motor gone awry. In fact, local legend has it that the fish was discovered by its terrible noises. Houseboat residents in the 1980s on the northeast end of the San Francisco Bay complained of loud droning sounds that interrupted their sleep. At first, they speculated it could be secret military operations like submarine tests or radar, but it was in fact the mating calls of hundreds of midshipman fish. This is one melody that we humans just can’t appreciate seem to appreciate!
Sweet sonic symphony of the plainfin midshipman fish.
How does the midshipman fish produce sound if it doesn’t have lungs like terrestrial animals? Just like birds, mammals and frogs that modulate air flow from the lungs through vibratory structures (like the larynx, syrinx, and air sacs), these fish contract muscles around their swim bladder, an air-filled organ that controls buoyancy. Studies of the brains of these fish has shown that the same neural circuits they use to regulate pressures in the swim bladder during swimming have been co-opted to also regulate sound production. The midshipman fish song also includes a series of repeated “grunts” that may be produced by the fish grinding its teeth together, a behavior called stridulation.
The coastal intertidal zone serves as an amphitheater for plainfin midshipman calls during breeding season. Pictured: Cabrillo State Park, CA. [Source]
Interestingly, female fish are more receptive or “in the mood” to hear the males’ songs as the breeding season approaches (month of May in Northern California). This is more than an urge to play the midshipman greatest hits on repeat! Their ears actually get physically more sensitive to these frequencies of the males’ sounds. In a study by Dr. Andrew Bass* at Cornell, a researcher examining the fascinating biology of these fish, sex hormones were found to increase in females to prepare them for the breeding season; females also began to grow hair cells in their inner ears to better hear the males. To solidify this relationship between hormones and ear cells, Dr. Bass injected estradiol (the “female” sex hormone) into non-breeding females, and the hair cells in their ears notably increased. This elegant mechanism allows the females to pay better attention to the males when it would be most relevant to do so: when they are reproductively active.
Dr. Bass was also interested to see if the muscles around the swim bladder, which allow it to vibrate to produce song, changed size in the males during the breeding season. While dissecting fish to compare male and female muscle sizes, he found that some fish he had pegged as “female” actually had male organs inside! These males were unable to sing, although they were fully grown, and had small muscles around their swim bladders. These “type II” males represented an alternative mating strategy in the fish. Rather than expend all energy to droning across the Bay to get mates, these males would mimic females and “sneak” fertilizations of eggs while just hanging out with the females. Unlike the vocal “type I” males, however, these “sneaker” males not only put less effort into singing, but also put in no effort to guard the nest of eggs once they were fertilized. A study of the hormones circulating in these males found that the type I males have high levels of a modified testosterone (the “male” sex hormone) that has stronger effects on the body, where as the type II males have predominantly “regular” unmodified testosterone. Scientists believe this difference in hormone profiles leads to the differences between male strategies.
This figure illustrates the swim bladder and gonad sizes of the two male types and the female plainfin midshipman. [Source]
Overall, studies of this bizarre singing fish have augmented what researchers know about sexual signaling in “higher-order” land animals. Studying fish, which have been living in the oceans for millions of years before lung-bearers colonized land, allows scientists to see what hormonal mechanisms may be shared by all vertebrates. The neural studies of the plainfin midshipman add exciting new insights to the age-old literature of song in birds and frogs, illustrating the importance of biodiversity both on earth and in the lab.
*How appropriate for a scientist studying fish! An undergraduate professor of mine once observed that scientists’ names often serendipitously match their study organism. For example, when I learned that much of the seminal work on bird hormones was done by UC Davis’ own Dr. John Wingfield, I was inclined to agree!
Bass, A.H. (1990) Sounds from the intertidal zone: Vocalizing Fish. Bioscience 40(4): 249-258. Retrieved from https://www.jstor.org/stable/pdf/1311261.pdf?refreqid=excelsior%3Af2eeaa758fc674c1544446bccadf7ac4
Bazell, R. & Gumbel, B. (1986) Humming Toadfish are the buzz of Sausalito [Television series episode]. NBC Today Show. Retrieved from https://archives.nbclearn.com/portal/site/k-12/browse/?cuecard=40085
Brantley, R. K. , Wingfield, J.C. , and Bass, A.H. (1993) Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism amongst teleost fishes. Hormones and Behavior 27(3): 332-347
Sisneros, J.A. (2009) Adaptive hearing in the vocal plainfin midshipman fish: getting in tune for the breeding season and implications for acoustic communication. Integrative Zoology 4:33-42. Retrieved from https://faculty.washington.edu/sisneros/Sisneros%20IZ%202009.pdf
Main featured image [Source]