Sonic Motor Pathways in Piranhas with a Reassessment of Phylogenetic Patterns of Sonic Mechanisms among TeleostsLadich F.a · Bass A.H.b
aDepartment of Neurobiology and Behavior, University of Vienna, Vienna, Austria; bDepartment of Neurobiology and Behavior, Cornell University, Ithaca, N.Y., USA
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
Article / Publication Details
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.
© 2005 S. Karger AG, Basel
- Barber SB, Mowbray WH (1956) Mechanism of sound production in the sculpin. Science 124:219–220.
- Bass AH (1985) Sonic motor pathways in teleost fishes: a comparative HRP study. Brain Behav Evol 27:115–131.
- Bass AH, Baker R (1990) Sexual dimorphism in the vocal control system of teleost fish: morphology of physiologically identified neurons. J Neurobiol 21:1155–1168.
- Bass AH, Baker R (1991) Evolution of homologous vocal control traits. Brain Behav Evol 38:240–254.
- Bass AH, Baker R (1997) Phenotypic specification of hindbrain rhombomeres and the origin of rhythmic circuits in vertebrates. Brain Behav Evol 50:3–16.
- Bass AH, Horvath BJ, Brothers E (1996) Nonsequential developmental trajectories lead to dimorphic vocal circuitry for males with alternative reproductive tactics. J Neurobiol 30:493–504.
- Bass AH, Marchaterre MA, Baker R (1994) Vocal-acoustic pathways in a teleost fish. J Neurosci 14:4025–4039.
- Carlson BA, Bass AH (2000) Sonic/vocal motor pathways in squirrelfish (Teleostei, Holocentridae). Brain Behav Evol 56:14–28.
- Crawford JD, Huang X (1999) Communication signals and sound production mechanisms of mormyrid electric fish. J Exp Biol 202:1417–1426.
Fine ML, Ladich F (2003) Sound production, spine locking and related adaptations. In: Catfishes, Vol. 1. (Arratia G, Kapoor BG, Chardon M, Diogo R, eds), pp 249–290, Enfield, NH: Science Publishers.
Fine ML, King CB, Friel JP, Loesser KE, Newton S (1999) Sound production and locking of the pectoral spine of the channel catfish. Am Fish Soc Symp 24:105–114.
Finger TE, Kalil K (1985) Organization of motoneuronal pools in the rostral spinal cord of the sea robin, Prionotus carolinus. J Comp Neurol239:384–390.
Fink SV, Fink WL (1996) Interrelationships of ostariophysan fishes. In: Interrelationships of Fishes (Stiassny MLJ, Pasenti LR, Johnson GD, eds), pp 209–249. San Diego: Academic Press.
- Fish MP (1953) The production of underwater sounds by the northern seahorse, Hippocampus hudsonius. Copeia 1953:98–99.
- Goodson JL, Bass AH (2002) Vocal-acoustic circuitry and descending vocal pathways in teleost fish: convergence with terrestrial vertebrates reveals conserved traits. J Comp Neurol 448:298–322.
Hallacher LE (1974) The comparative morphology of extrinsic gasbladder musculature in the scorpionfish Genus Sebastes (Pisces: Scorpaenidae). Proc Cal Acad Sci 40:59–86.
Hawkins AD (1993) Underwater sound and fish behaviour. In: Behaviour of Teleost Fishes. (Pitcher TJ, ed), pp 129–169. London: Chapman and Hall.
- Johnston CE, Johnson DL (2000) Sound production in Pimephales notatus (Rafinesque) (Cyprinidae). Copeia 2000:567–571.
Kastberger G (1981a) Economy of sound production in piranhas (Serrasalminae, Characidae): I. Functional properties of sonic muscles. Zool Jahrb Physiol 85:113–125.
Kastberger G (1981b) Economy of sound production in piranhas (Serrasalminae, Characidae): II. Functional porperties of sound emitter. Zool Jahrb Physiol 85:393–411.
- Kratochvil H (1978) Der Bau des Lautapparates vom Knurrenden Gurami (Trichopsis vittatus Cuvier & Valenciennes) (Anabantidae, Belontiidae). Zoomorphologie 91:91–99.
- Ladich F (1988) Sound production by the gudgeon, Gobio gobio L., a common European freshwater fish (Cyprinidae, Teleostei). J Fish Biol 32:707–715.
- Ladich F (1989) Sound production by the river bullhead Cottus gobio L. (Cottidae, Teleostei). J Fish Biol 35:531–538.
Ladich F (1997) Comparative analysis of swimbladder (drumming) and pectoral (stridulation) sounds in three families of catfishes. Bioacoustics 8:85–208
- Ladich F (1999) Did auditory sensitivity and vocalization evolve independently in otophysan fishes? Brain Behav Evol 53:288–304.
- Ladich F (2001) Sound-generating and -detecting motor system in catfish: design of swim bladder muscles in doradids and pimelodids. Anat Rec 263:297–306.
Ladich F (2004) Sound production and acoustic communication. In: The Senses of Fishes. Adaptations for the Reception of Natural Stimuli. (Van der Emde G, Mogdans J, Kapoor BG, eds), pp 210–230. New Delhi: Narosa Publ House.
- Ladich F, Bass AH (1996) Sonic/vocal-acousticolateralis pathways in teleost fishes: a transneuronal neurobiotin study in mochokid catfish. J Comp Neurol 374:493–505.
- Ladich F, Bass AH (1998) Sonic/vocal motor pathways in catfishes: comparison with other teleosts. Brain Behav Evol 51:315–330.
Ladich F, Bass AH (2003) Underwater sound generation and acoustic reception in fishes with some notes on frogs. In: Sensory Processing in Aquatic Environments (Collin SP, Marshall NJ, eds), pp 173–193. New York: Springer.
- Ladich F, Fine ML (1992) Localization of pectoral fin motoneurons (sonic and hovering) in the croaking gourami Trichopsis vittatus. Brain Behav Evol 39:1–7.
- Ladich F, Fine ML (1994) Localization of swim bladder and pectoral motoneurons involved in sound production in pimelodid catfish. Brain Behav Evol 44:86–100.
Ladich F, Fine ML (in press) Sound generating mechanisms. In: Fish Communication (Ladich F, Collin SP, Moller P, Kapoor BG, eds). New Delhi: Narosa Publ. House.
- Lanzing, WSR (1974) Sound production in the cichlid Tilapia mossambica Peters. J Fish Biol 6:341–347.
- Lindholm MM, Bass AH (1993) Early events in myofibrillogenesis and innervation of skeletal sound-generating muscle in a teleost fish. J Morphol 216:225–239.
Lundberg JG (1993) African-South American freshwater fish clades and continental drift: problem with a paradigma. In: Biological Relationship Between Africa and South America (Goldblatt P, ed), pp 156–199. New Haven CT: Yale Univ Press.
- Markl H (1971) Schallerzeugung bei Piranhas (Serrasalminae, Characidae). Z Vergl Physiol 74:39–56.
Nelson JS (1994) Fishes of the World (3rd ed). New York: John Wiley and Sons.
- Ono RD, Poss SG (1982) Structure and innervation of the swim bladder musculature in the weakfish, Cynoscion regalis (Teleostei: Sciaenidae). Can J Zool 60:1955–1967.
Rauther M (1945) İber die Schwimmblase und die zu ihr in Beziehung tretenden somatischen Muskeln bei den Trigliden und anderen Scleroparei. Zool Jahrb Anat 69:159–250.
Salmon M, Winn HE, Sorgente N (1968) Sound production and acoustical behavior in triggerfish. Pac Sci 12:11–20.
Schaller F, Kratochvil H (1981) Lautbildung bei Fischen. Biologie in unserer Zeit 11:43–47.
- Schneider H (1964) Physiologische und morphologische Untersuchungen zur Bioakustik der Tigerfische (Pisces, Theraponidae). Z Vergl Physiol 47:493–558.
- Stabentheiner A (1988) Correlations between hearing and sound production in piranhas. J Comp Physiol A 162:67–76.
- Stout JF (1963) The significance of sound production during the reproductive behaviour of Notropis analostanus (Family Cyprinidae). Anim Behav 11:83–92.
- Takayama M, Onuki A, Yosino T, Yoshimoto M, Ito H, Kohbara J, Somiya H (2003) Sound characteristics and the sound producing system in silver sweeper, Pempherisschwenkii (Perciformes: Pempheridae). J Mar Biol Assoc UK 83:4062/1–4.
Tavolga WN (1962) Mechanism of sound production in the ariid catfish Galeichthys and Bagre. Bull Am Mus Nat Hist 24:1–30.
- Tracy HC (1959) Stages in the development of the anatomy of motility of the toadfish (Opsanus tau). J Comp Neurol 111:27–81.
- Tracy HC (1961) Development of the spinal crest, nerves and muscles in the toadfish (Opsanus tau). J Comp Neurol 116:291–315.
- Vance TL, Hewson JM, Modla S, Connaughton MA (2002) Variability in sonic muscle size and innervation among three sciaenids: spot, Atlantic croaker, and weakfish. Copeia 2002:1137–1143.
Wilson B, Batty RS, Dill LM (2004) Pacific and Atlantic herring produce bursts pulse sounds. Proc R Soc Lond B (suppl) 271:95–97.
Winn HE, Marshall JA (1963) Sound-producing organ of the squirrelfish, Holocentrus rufus. Physiol Zool 36:36–44.
- Yoshimoto M, Kikuchi K, Yamamoto N, Somiya H, Ito H (1999) Sonic motor nucleus and its connections with octaval and lateral line nuclei of the medulla in a rockfish, Sebastiscus marmoratus. Brain Behav Evol 54:183–204.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.