Abstract: Development of the vocal-auditory systems for social communication in a teleost fish
Raquel O. Vasconcelos1, Paulo J. Fonseca2, M. Clara P. Amorim3, and Joseph A. Sisneros4
1Institute of Science and Environment, University of Saint Joseph, Macau S.A.R., People’s Republic of China.
2Departamento de Biologia Animal, Centre for Ecology, Evolution and Environmental Changes, Universidade de Lisboa, Portugal.
3MARE – Marine and Environmental Sciences Centre, ISPA – Instituto Universitário, Lisbon, Portugal.
4Departments of Psychology and Biology, University of Washington, WA, USA.
A fundamental question for all vocal communication systems concerns the relationship between the developmental processes of vocal differentiation and auditory perception during ontogenetic development. Such developmental processes have been well documented in birds and mammals but poorly investigated in other vertebrates. Fish represent the oldest and largest extant vertebrate group. Besides, neural circuitry controlling vocal behavior is thought to have evolved from conserved brain areas that originated in this taxon, which makes this group key to understanding the evolution and development of the vertebrate vocal-auditory systems. However, the relationship between the vocal motor and auditory systems during development for social communication in fish remains unclear.
The goals of this study were: 1) examine how vocal behavior develops during ontogeny; and 2) compare auditory sensitivity of the saccule (main auditory endorgan) across developmental stages in the Lusitanian toadfish, Halobatrachus didactylus (Batrachoididae). This teleost species has become an interesting model to investigate questions related to vocal communication due to its unusual complex vocal repertoire and early vocal onset. Vocalizations were recorded during social interactions for four size groups (fry: <2 cm; small juveniles: 2–4 cm; large juveniles: 5–7 cm; adults >25 cm, standard length). Auditory sensitivity of juveniles and adults was determined based on evoked potentials recorded from populations of saccular hair cells in response to pure tones of 75–945 Hz.
We found an ontogenetic increment in the vocal repertoire from simple broadband-pulsed ‘grunts’ that later differentiate into four distinct vocalizations, including low-frequency amplitude-modulated ‘boatwhistles’. Whereas fry emitted mostly single grunts, large juveniles exhibited vocalizations similar to the adult vocal repertoire. Moreover, we showed that the number of stereotyped vocalizations increased in large juveniles above 5 cm SL, which was coincident with an increase in saccular auditory sensitivity. Saccular sensitivity revealed a three-fold enhancement at most frequencies tested from small to large juveniles; and large juveniles were similar in sensitivity to adults.
This study provides first clear evidence of ontogenetic development of the vocal repertoire in fish, as previously described for higher vertebrates. The results suggest a parallel development between the vocal motor pathway and the peripheral auditory system in fish. We suggest that this parallel development may serve an important and conserved function in the development of social acoustic communication among vertebrates.