Sonic Motor Pathways in Piranhas with a Reassessment of Phylogenetic Patterns of Sonic Mechanisms among Teleosts

Abstract

Sound production has evolved independently a number of times among teleost fishes. In most cases, sound is generated by fast contracting muscles that vibrate the swim bladder by way of their direct attachment (intrinsic muscles) or indirectly by way of other skeletal elements (extrinsic muscles). This study focuses on the red and black piranha, Pygocentrus nattereri and Serrasalmus rhombeus (superorder Ostariophysi, Order Characiformes), that have extrinsic swim bladder sonic muscles innervated by the third and fourth spinal nerves. This innervation pattern diverges from that found in most teleosts, including the closely related catfishes (Ostariophysi, Siluriformes), where sonic muscles are innervated by ventral occipital nerve roots that arise just caudal to the vagus nerve. Here, we tested the hypothesis that piranhas would also differ from most other teleosts in the location of their sonic motor neurons. Following biotin labeling of branches of the third and fourth spinal nerves that innervate the sonic muscles in the red and black piranha, sonic motor neurons were identified amongst other non-sonic motor neurons in the central part of the spinal cord, slightly ventrolateral to the central canal. To our knowledge, this is the first example of sonic motor neurons positioned entirely within the spinal cord. In the other species so far studied, sonic motor neurons form well-defined nuclei that extend from far caudal levels of the medulla into the rostral spinal cord and are located either within the ventral motor column or near the midline, close to or just ventrolateral to the fourth ventricle and central canal. A piranha-like pattern may be more widespread among characiforms and is likely present in other teleost orders, e.g., Sciaenidae (drumfishes), that also have sonic muscles innervated by spinal nerves.

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

“…Markl (Markl, 1971) and Kastberger (Kastberger, 1981a) found that drumming calls of hand-held specimens consisted of low-frequency harmonic sounds with several pulses and with a period of 7-10ms. These sounds are generated by rapid contractions of sonic muscles, which originate on transverse expansions at the base of the second rib and insert on a broad tendon that ventrally surrounds the cranial sac of the swimbladder (Ladich and Bass, 2005). The sonic muscles are round in shape, extend between the first and third ribs (Ladich and Bass, 2005) and are innervated by branches of the third, fourth and fifth spinal nerves (Onuki et al, 2006).…”

“…These sounds are generated by rapid contractions of sonic muscles, which originate on transverse expansions at the base of the second rib and insert on a broad tendon that ventrally surrounds the cranial sac of the swimbladder (Ladich and Bass, 2005). The sonic muscles are round in shape, extend between the first and third ribs (Ladich and Bass, 2005) and are innervated by branches of the third, fourth and fifth spinal nerves (Onuki et al, 2006). Sounds result from fastcontracting sonic muscles, whose contraction rate determines the pulse rate of the drumming sounds (Kastberger, 1981a), which also showed harmonics (Kastberger, 1981b).…”

Shared developmental and evolutionary origins for neural basis of vocal–acoustic and pectoral–gestural signaling

“…Occipital innervation of vocal muscles originating from a VMN at the same hindbrain (rh8)-spinal level is now documented for nine families of closely and distantly related teleost taxa (20,25,55,56) (57).…”

“…1A) (24) and pectoral girdle vibration in sculpin that lack a swim bladder (25). Despite these divergent mechanisms, sonic motoneurons are positioned in the same hindbrain-spinal region of the pectoral motor column in sculpin (25,55), catfish (80,81), and gouramis (82). Sonic neurons map to the same location in sea robins, close relatives of sculpin that have sonic muscles completely attached to the swim bladder as in distantly related toadfishes (25).…”

Spinal Nerve Innervation to the Sonic Muscle and Sonic Motor Nucleus in Red Piranha, <i>Pygocentrus nattereri</i> (Characiformes, Ostariophysi)

“…1998; Yoshimoto et al, 1999;Carlson and Bass, 2000;Bass and McKibben, 2003;Takayama et al, 2003] indicate that no investigation of the detailed innervation pattern of the sonic muscles of the piranha has been conducted [see also Ladich and Bass, 2005]. Also, studies on the distribution of the sonic motor neurons that innervate the sonic muscles via the spinal nerves are lacking.…”