Sound production in red-bellied piranhas (Pygocentrus nattereri, Kner): an acoustical, behavioural and morphofunctional study

Abstract

SUMMARYPiranhas are known to be sound-producing animals. Nevertheless, the biological significance of piranha calls remains unclear because sounds have been recorded only when specimens were held by hand or trapped in a gill net. These sounds are generated by rapid contractions of sonic muscles that insert on a broad tendon surrounding ventrally the cranial sac of the swimbladder. The piranha swimbladder is thought to play an important role in sound production as an impedance-matching device and as a resonator. However, the vibratory capacities of the cranial and caudal sacs and the exact role of both sacs in sound production remain poorly understood. In this study, three sounds were each associated to a specific behaviour. The first sound (type 1) was produced during frontal display; it had numerous pulses and lasted 140±17ms, with a fundamental frequency of 120±4Hz. It corresponded to the sound made by hand-held fishes. The second sound (type 2) was produced during circling and fighting behaviour; it was a single pulse lasting 36±8ms, with a fundamental frequency of 43±10Hz. The third sound (type 3) corresponded to chasing behaviour and comprised three to four pulses, each lasting 3±1ms, with a fundamental frequency of 1739±18Hz. Using a laser vibrometer to study the swimbladder displacement when stimulated at different frequencies, it was demonstrated that the first two sounds corresponded to the swimbladder mechanism. By contrast, the third sound was associated with the jaw mechanism. The vibrometer indicated that the swimbladder is a highly damping structure, simply copying the sonic muscle contraction rate. This study provides two interesting insights. First, it shows the relationships between three kinds of piranha sound and three specific behaviours. Second, using muscle stimulation at different rates, it shows which simultaneous conditions are required for production of sound in this species. Swimbladder calls were produced by a muscle contraction rate of approximately 100Hz because this periodicity allowed the swimbladder to vibrate. At this frequency range, the contraction-relaxation cycles of the swimbladder muscles engendered wall displacements that had short amplitudes and with only a small variability between them.

A superfast muscle in the complex sonic apparatus of Ophidion rochei (Ophidiiformes): histological and physiological approaches

“…20 μm in diameter) that are not completely tetanized at 500 Hz (Fine et al, 1990;Fine et al, 2001). Fast contracting sonic muscles were also described in Pygocentrus nattereri (Millot et al, 2011) and several holocentrid species (Gainer A superfast muscle in the complex sonic apparatus of Ophidion rochei (Ophidiiformes): histological and physiological approaches et al, 1965;Parmentier et al, 2011). Again, superfast activity appears to be paralleled by the typical fast fiber morphology (Gainer et al, 1965;Eichelberg, 1977;Parmentier et al, 2011).…”

“…Again, superfast activity appears to be paralleled by the typical fast fiber morphology (Gainer et al, 1965;Eichelberg, 1977;Parmentier et al, 2011). In O. tau, P. nattereri and Holocentrus rufus, the fundamental frequency of the sound corresponds to the contraction rate of the sonic muscle (Fine et al, 2001;Millot et al, 2011). In Carapus acus (Carapidae), Parmentier et al (Parmentier et al, 2006a) demonstrated that sonic muscles inserting on the swimbladder can also produce sounds at very low contraction rates (sonic muscle tetanized between 10 and 20 Hz).…”

“…In vertebrates, these muscles are always associated with sound production and are known from some species of snakes (Rome et al, 1996), birds (Elemans et al, 2008), bats (Elemans et al, 2011), and fishes (Tavolga, 1964;Millot et al, 2011). The contraction rate of superfast muscles determines the fundamental frequency of the sound in fish (Skoglund, 1961;Fine et al, 2001;Millot et al, 2011), allows rapid modulations of sound RESEARCH ARTICLE characteristics in birds (Elemans et al, 2008), and sets the call rate in echolocating bats (Elemans et al, 2011). Rome et al (Rome et al, 1996) also considered that rattlesnake tail shaker muscles are used 'to produce sounds at the frequency at which the muscle contracts'.…”

New insights into the role of the pharyngeal jaw apparatus in the sound-producing mechanism of Haemulon flavolineatum (Haemulidae)

“…In the case of Haemulon, we hypothesize that the sounds made during food processing are secondarily selected to support acoustic communication. This hypothesis of exaptation between feeding mechanism and sound production has already been formulated by Parmentier et al (Parmentier et al, 2007) for the slam jaw mechanism in the clownfish Amphiprion clarkii and in the piranha Pygocentrus nattereri in which some sounds are produced when a fish snaps its jaws to bite a conspecific (Millot et al, 2011).…”

Further insight into the sound-producing mechanism of clownfishes: what structure is involved in sound radiation?

“…Thereby, such examples raise questions regarding the resonating structure involved in the sound-producing mechanism of clownfishes. However, it was recently shown in the oyster toadfish (Fine et al, 2009) and in the red-bellied piranha (Millot et al, 2011) that the swimbladder was a highly damped structure, prevented from sustained resonant vibrations.…”