Animals experience interesting seasonal transformations, such as the thick fur that animals in the Arctic grow in the winter. This phenomenon can also extend to vocal systems. The plainfin midshipman fish, found along the North American coast of the Pacific Ocean during summer, undergo seasonal changes in their swim bladder. Swim bladders are gas-filled organs that most fish use for buoyancy; however, plainfin midshipman vibrate the organs to produce distinctive sounds for communication. The male fish hum to the females during the breeding season and these calls are supported by the muscles around the bladder that develop before the summer. In addition, the swim bladder helps them to hear the calls of other chatty fish in the vicinity by transmitting sounds that they then pick up with their ears. But how much does the structure of the swim bladder change in the months leading up to, and during, the mating season and how do these changes affect the fish's hearing and the sounds they produce? A recent study by Joseph Sisneros and colleagues at the University of Washington and Seattle Children's Research Institute, USA, addresses these questions.
In their investigation, Sisneros and colleagues gathered fish from Puget Sound, USA, during February 2022 when the fish were not breeding and again between May and June, during the fish's breeding season. They then used X-ray-based CT scans to closely examine changes in the fish's swim bladder over the months. Sure enough, the swim bladder changed size and shape with the season. In February, the swim bladders of the non-reproductive males had horn-like extensions that brought the swim bladder closer to the fish's inner ear, enhancing their sensitivity to low-frequency (less than 800 Hz) sounds. In contrast, during the mating season in May and June, the males had three times more muscle mass around the bladder, enabling them to sing and call to females for longer. However, this increase in muscle mass also altered the shape of the swim bladder – increasing its width, while shortening the length – increasing the distance to the inner ear, which could reduce the sensitivity of the fish's hearing in the summer.
In a follow-up experiment, the researchers checked the hearing of the fish to find out how the organ contributes to their hearing over the seasons. They found that the hearing of the non-breeding males in February is enhanced (12.5 times more sensitive than the hearing of non-breeding males without a swim bladder) and tuned to sounds in the environment. In contrast, when they removed the swim bladder from breeding males and compared their hearing with that of intact breeding males, their hearing was unaffected. The breeding fish were not using their swim bladders to help them pick up sound, probably to protect their hearing from their own droning 2-hour-long serenades while courting females.
Lastly, Sisneros and the team tried to mimic how the swim bladder vibrates, to understand how well the swim bladder is tuned to produce sounds in one season while contributing to hearing in another. The researchers did this by building a model of the breeding and the non-breeding fish's swim bladders in a computer simulation and then calculating how the structures would vibrate. This showed that the swim bladder of the breeding male midshipman fish is tuned to produce the low frequency social calls – hums, grunts and growls – that they use during courtship. On the flip side, non-breeding males in February have swim bladders that are geared towards higher frequency sounds, tuning their hearing to the ambient sounds in the ocean.
It seems that the male plainfin midshipman swim bladder adapts to the seasons: fine-tuning the fish's hearing to listen out for sounds in the surrounding water out of the breeding season and building up to produce amorous courtship serenades during the breeding season, while also protecting their own hearing from their droning vocal performance. So male plainfin midshipman have expanded the swim bladder's repertoire from simple buoyancy aid to hearing aid and vocal box by modifying the organ through the seasons.
