Vocal–Acoustic Communication in Fishes: Neuroethology

For seasonally breeding vertebrates, reproductive cycling is often coupled with changes in vocalizations that function in courtship and territoriality. Less is known about changes in auditory sensitivity to those vocalizations. Here, we show that nonreproductive female midshipman fish treated with either testosterone or 17beta-estradiol exhibit an increase in the degree of temporal encoding of the frequency content of male vocalizations by the inner ear that mimics the reproductive female's auditory phenotype. This sensory plasticity provides an adaptable mechanism that enhances coupling between sender and receiver in vocal communication.

The macroevolutionary events leading to neural innovations for social communication, such as vocalization, are essentially unexplored. Many fish vocalize during female courtship and territorial defense, as do amphibians, birds, and mammals. Here, we map the neural circuitry for vocalization in larval fish and show that the vocal network develops in a segment-like region across the most caudal hindbrain and rostral spinal cord. Taxonomic analysis demonstrates a highly conserved pattern between fish and all major lineages of vocal tetrapods. We propose that the vocal basis for acoustic communication among vertebrates evolved from an ancestrally shared developmental compartment already present in the early fishes.

The passive listening hypothesis proposes that dolphins and whales detect acoustic signals emitted by prey, including sound-producing (soniferous) fishes. Previous work showed that bottlenose dolphins (Tursiops truncatus) behaviorally orient toward the sounds of prey, including the advertisement calls of male Gulf toadfish (Opsanus beta). In addition, soniferous fishes constitute over 80% of Tursiops diet, and toadfishes alone account for approximately 13% of the stomach contents of adult bottlenose dolphins. Here, we used both behavioral (vocalizations) and physiological (plasma cortisol levels) parameters to determine if male Gulf toadfish can, in turn, detect the acoustic signals of bottlenose dolphins. Using underwater playbacks to toadfish in their natural environment, we found that low-frequency dolphin sounds (;pops') within the toadfish's range of hearing dramatically reduce toadfish calling rates by 50%. High frequency dolphin sounds (whistles) and low-frequency snapping shrimp pops (ambient control sounds) each had no effect on toadfish calling rates. Predator sound playbacks also had consequences for circulating stress hormones, as cortisol levels were significantly elevated in male toadfish exposed to dolphin pops compared with snapping shrimp pops. These findings lend strong support to the hypothesis that individuals of a prey species modulate communication behavior in the presence of a predator, and also suggest that short-term glucocorticoid elevation is associated with anti-predator behavior.