Abstract

BackgroundDrumming muscles of some sound-producing fish are ‘champions’ of contraction speed, their rate setting the fundamental frequency. In the piranha, contraction of these muscles at 150 Hz drives a sound at the same frequency. Drumming muscles of different not closely related species show evolutionary convergences. Interestingly, some characters of sonic muscles can also be found in the trunk muscles of newly hatched larvae that are able to maintain tail beat frequencies up to 100 Hz. The aim of this work was to study the development of sound production and sonic and epaxial muscles simultaneously in the red bellied piranhas (Pygocentrus nattereri) to seek for possible common characteristics.ResultsCall, pulse and period durations increased significantly with the fish size, but the call dominant frequencies decreased, and the number of pulses and the call amplitude formed a bell curve. In epaxial muscles, the fibre diameters of younger fish are first positioned in the graphical slope corresponding to sonic muscles, before diverging. The fibre diameter of older fish trunk muscles was bigger, and the area of the myofibrils was larger than in sonic muscles. Moreover, in two of the biggest fish, the sonic muscles were invaded by fat cells and the sonic muscle ultrastructure was similar to the epaxial one. These two fish were also unable to produce any sound, meaning they lost their ability to contract quickly.ConclusionsThe volume occupied by myofibrils determines the force of contraction, the volume of sarcoplasmic reticulum sets the contraction frequency, and the volume of mitochondria sets the level of sustained performance. The functional outcomes in muscles are all attributable to shifts in the proportions of those structures. A single delay in the development restricts the quantity of myofibrils, maintains a high proportion of space in the sarcoplasm and develops sarcoplasmic reticulum. High-speed sonic muscles could thus be skeletal muscles with delayed development. This hypothesis has the advantage that it could easily explain why high-speed sonic muscles have evolved so many times in different lineages.

Highlights

  • Drumming muscles of some sound-producing fish are ‘champions’ of contraction speed, their rate setting the fundamental frequency

  • Fish species have developed different mechanisms allowing them to produce sounds. Those involving the use of fast sound producing muscles [1,2] and swim bladders can be roughly divided into four groups: 1) those whose muscles are directly inserted on areas covering important parts of the swimbladder, such as in the toadfish taxa [3,4,5,6], the searobin [7] or pimelodids [8,9]; 2) those whose muscles possess ventral tendons running from the left to the right sonic muscles, such as in piranhas [10,11,12], 3) those whose muscles lie on the body wall and extend

  • The cell space was mainly occupied by the nucleus, and the ultrastructure was characterized by scarce myofibrillar packs as small as mitochondria (Figure 2A)

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Summary

Introduction

Drumming muscles of some sound-producing fish are ‘champions’ of contraction speed, their rate setting the fundamental frequency. Fish species have developed different mechanisms allowing them to produce sounds Those involving the use of fast sound producing muscles [1,2] and swim bladders can be roughly divided into four groups: 1) those whose muscles are directly inserted on areas covering important parts of the swimbladder, such as in the toadfish taxa [3,4,5,6], the searobin [7] or pimelodids [8,9]; 2) those whose muscles possess ventral tendons running from the left to the right sonic muscles, such as in piranhas [10,11,12], 3) those whose muscles lie on the body wall and extend. According to Ladich and Bass [11], in piranhas (characiform) it seems unlikely that sonic muscles derive from occipital somites because their innervation is accomplished by true spinal nerves

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