[en] In fshes, sonic abilities for communication purpose usually involve a single mechanism. We describe here the sonic mechanism and sounds in two species of boxfsh, the spotted trunkfsh Ostracion meleagris and the yellow boxfsh Ostracion cubicus. The sonic mechanism utilizes a T-shaped swimbladder with a swimbladder fenestra and two separate sonic muscle pairs. Extrinsic vertical muscles attach to the vertebral column and the swimbladder. Perpendicularly and below these muscles, longitudinal intrinsic muscles cover the swimbladder fenestra. Sounds are exceptional since they are made of two distinct types produced in a sequence. In both species, humming sounds consist of long series (up to 45s) of hundreds of regular low-amplitude pulses. Hums are often interspersed with irregular click sounds with an amplitude that is ten times greater in O. meleagris and forty times greater in O. cubicus. There is no relationship between fsh size and many acoustic characteristics
because muscle contraction rate dictates the fundamental frequency. We suggest that hums and clicks
are produced by either separate muscles or by a combination of the two. The mechanism complexity
supports an investment of boxfsh in this communication channel and underline sounds as having
important functions in their way of life.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Solagna, Laura
Bertucci, Frédéric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Fine, Michael L.
Nakae
Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Smeets, Sarah ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Raick, Xavier ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Lecchini, David
Language :
English
Title :
Simultaneous production of two kinds of sounds in relation with sonic mechanism in the boxfsh Ostracion meleagris and O. cubicus
Ruppé, L. et al. Environmental constraints drive the partitioning of the soundscape in fishes. Proc. Natl. Acad. Sci. 112, 6092–6097 (2015).
Fine, M. L. & Parmentier, E. Mechanisms of fish sound production. In Sound Communication in Fishes. (ed. Ladich, F.) 77–126 (Springer, 2015).
Slabbekoorn, H. et al. A noisy spring: The impact of globally rising underwater sound levels on fish. Trends Ecol. Evol. 25, 419–427 (2010).
Picciulin, M., Sebastianutto, L., Codarin, A., Calcagno, G. & Ferrero, E. A. Brown meagre vocalization rate increases during repetitive boat noise exposures: a possible case of vocal compensation. J. Acoust. Soc. Am. 132, 3118–3124 (2012).
Vasconcelos, R. O., Amorim, M. C. P. & Ladich, F. Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish. J. Exp. Biol. 210, 2104 LP–2112 (2007).
Tricas, T. C. & Boyle, K. S. Acoustic behaviors in Hawaiian coral reef fish communities. Mar. Ecol. Prog. Ser. 511, 1–16 (2014).
Lobel, P. S., Kaatz, I. M. & Rice, A. N. Acoustic behaviour of coral reed fish. In Reproduction and sexuality in marine fishes: patterns and procesess (ed. Cole, K. S.) 307–386 (University of California Press, 2010).
Lobel, P. S. The “Choral Reef”: the ecology of underwater sounds. In Joint International Scientific Diving Symposium AAUS & ESDP. (eds Lang, M. A. & Sayer, M.) 179–184 (2013).
Matsuura, K. Taxonomy and systematics of tetraodontiform fishes: a review focusing primarily on progress in the period from 1980 to 2014. Ichthyol. Res. 62, 72–113 (2015).
Myers, R. F. Micronesian Reef Fishes. (Coral Graphics, 1999).
Sancho, G., Solow, A. R. & Lobel, P. S. Environmental influences on the diel timing of spawning in coral reef fishes. Mar. Ecol. Prog. Ser. 206, 193–212 (2000).
Sancho, G. Factors regulating the height of spawning ascents in trunkfishes (Ostraciidae). J. Fish Biol. 53, 94–103 (1998).
Cornic, A. Poissons de l’Ile Maurice. (1987).
Debelius, H. Guide du Récif Corallien. Mer Rouge. (PLB Editions, 1998).
Moyer, J. T. Mating strategies and reproductive behavior of ostraciid fishes at Miyake-jima, Japan. Japanese J. Ichthyol. 26, 148–160 (1979).
Lobel, P. S. Spawning sound of the trunkfish, Ostracion meleagris (Ostraciidae). Biol. Bull. 191, 308–309 (1996).
Mann, D. & Lobel, P. S. Acoustic behaviour of the damselfish Dascyllus albisella: behavioural and geographic variation. Environ. Biol. Fishes 51, 421–428 (1998).
Parmentier, E. & Fine, M. L. Fish sound production: insights. In Vertebrate sound production and acoustic communication. (eds Suthers, R., Tecumseh, F., Popper, A. N. & Fay, R. R.) 19–49 (Springer, 2016).
Ladich, F. & Fine, M. L. Sound generating mechanisms in fishes: a unique diversity in vertebrates. In Communication in Fishes. (eds Ladich, F., Collin, S. P., Moller, P. & Kapoor, B. G.) 3–34 (Science Publishers, 2006).
Parmentier, E. & Diogo, R. Evolutionary trends of swimbladder sound mechanism in some teleost fishes. In Communication in Fishes. (eds Ladich, F., Collin, S. P., Moller, P. & Kapoor, B. G.) 45–70 (Science Publishers, 2006).
Fine, M. L., Malloy, K. L., King, C., Mitchell, S. L. & Cameron, T. M. Movement and sound generation by the toadfish swimbladder. J. Comp. Physiol. - A Sensory, Neural, Behav. Physiol. 187, 371–379 (2001).
Fine, M. L., King, T. L., Ali, H., Sidker, N. & Cameron, T. M. Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfish Opsanus tau. Proc. R. Soc. B Biol. Sci. 283, 20161094 (2016).
Chanet, B., Guintard, C. & Lecointre, G. The gas bladder of puffers and porcupinefishes (Acanthomorpha: Tetraodontiformes): Phylogenetic interpretations. J. Morphol. 275, 894–901 (2014).
Fish, M. P. & Mowbray, H. M. Sounds of Western North Atlantic Fishes (The Johns Hopkins Press, 1970).
Richardson, K. C., Jarett, L. & Finke, E. H. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).
Oliveira, T. P. R., Ladich, F., Abed-Navandi, D., Souto, A. S. & Rosa, I. L. Sounds produced by the longsnout seahorse: a study of their structure and functions. J. Zool. 294, 114–121 (2014).
Millot, S. & Parmentier, E. Development of the ultrastructure of sonic muscles: a kind of neoteny? BMC Evol. Biol. 14, 1–9 (2014).
Markl, H. Schallerzeugung bei Piranhas (Serrasalminae, Characidae). Z. Vgl. Physiol. 74, 39–56 (1971).
Parmentier, E., Vandewalle, P., Brié, C., Dinraths, L. & Lecchini, D. Comparative study on sound production in different Holocentridae species. Front. Zool. 8, 12 (2011).
Parmentier, E., Boyle, K. S., Berten, L., Brié, C. & Lecchini, D. Sound production and mechanism in Heniochus chrysostomus (Chaetodontidae). J. Exp. Biol. 214, 2702–2708 (2011).
Akamatsu, T., Okumura, T., Novarini, N. & Yan, H. Y. Empirical refinements applicable to the recording of fish sounds in small tanks. J. Acoust. Soc. Am. 112, 3073–3082 (2002).
Klassen, G. J. Phylogeny and biogeography of the Ostraciinae (Tetraodontiformes: Ostraciidae). Bulletin of Marine Science 57, 393–441 (1995).
Uehara, M., Hosaka, Y. Z., Doi, H. & Sakai, H. The shortened spinal cord in tetraodontiform fishes. J. Morphol. 276, 290–300 (2015).
Parmentier, E., Lecchini, D. & Mann, D. A. Sound production in damselfishes. In Biology of damselfishes. (eds Frédérich, B. & Parmentier, E.) 204–228 (CRC Press, Taylor & Francis, 2016).
Parmentier, É., Colleye, O. & Lecchini, D. New insights into sound production in Carapus mourlani (Carapidae). Bull. Mar. Sci. 92 (2016).
Onuki, A. & Somiya, H. Two types of sounds and additional spinal nerve innervation to the sonic muscle in John Dory, Zeus faber (Zeiformes: Teleostei). J. Mar. Biol. Assoc. UK 84, 843–850 (2004).
Bass, A. H. & Baker, R. Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons. J. Neurobiol. 21, 1155–1168 (1990).
Bass, A. H. & McKibben, J. R. Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog. Neurobiol. 69, 1–26 (2003).
Parmentier, E., Bouillac, G., Dragicevic, B., Dulcic, J. & Fine, M. Call properties and morphology of the sound-producing organ in Ophidion rochei (Ophidiidae). J. Exp. Biol. 213, 3230–3236 (2010).
Kéver, L. et al. Sexual dimorphism of sonic apparatus and extreme intersexual variation of sounds in Ophidion rochei (Ophidiidae): first evidence of a tight relationship between morphology and sound characteristics in Ophidiidae. Front. Zool. 9–34 (2012).
Kéver, L. et al. Sound production in Onuxodon fowleri (Carapidae) and its amplification by the host shell. J. Exp. Biol. 217, 4283–4294 (2014).
Rose, J. A. Anatomy and sexual dimorphism of the swim bladder and vertebral column in Ophidion holbrooki (Pisces: Ophidiidae). Bull. Mar. Sci. 11, 280–308 (1961).
Ali, H. A., Mok, H.-K. & Fine, M. L. Development and sexual dimorphism of the sonic system in deep sea neobythitine fishes: The upper continental slope. Deep Sea Res. Part I Oceanogr. Res. Pap. 115, 293–308 (2016).
Parmentier, E., Lagardère, J. P., Chancerelle, Y., Dufrane, D. & Eeckhaut, I. Variations in sound-producing mechanism in the pearlfish Carapini (Carapidae). J. Zool. 276, 266–275 (2008).
Parmentier, E., Bahri, M. A., Plenevaux, A., Fine, M. L. & Estrada, J. M. Sound production and sonic apparatus in deep-living cusk-eels (Genypterus chilensis and Genypterus maculatus). Deep Sea Res. Part I 141, 83-92 (2018)
Carlson, B. A. & Bass, A. H. Sonic/vocal motor pathways in squirrelfish (Teleostei, Holocentridae). Brain. Behav. Evol. 56, 14–28 (2000).
Yoshimoto, M., Kikuchi, K., Yamamoto, N., Somiya, H. & Ito, H. 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 (1999).
Onuki, A. & Somiya, H. Innervation of sonic muscles in teleosts: occipital vs. spinal nerves. Brain Behav. Evol. 69, 132–141 (2007).
Bass, A. H., Chagnaud, B. P. & Feng, N. Y. Comparative neurobiology of fishes. In Sound Communication in Fishes. Animal Signals and Communication. (ed. Ladich, F.) 35–75 (Springer, 2015).
Parmentier, E. et al. Functional study of the pectoral spine stridulation mechanism in different mochokid catfishes. J. Exp. Biol. 213, 1107–1114 (2010).
Ladich, F. Sound-generating and -detecting motor system in catfish: design of swimbladder muscles in doradids and pimelodids. Anat. Rec. 263, 297–306 (2001).
Ladich, F. Comparative analysis of swimbladder (drumming) and pectoral (stridulation) sounds in three families of catfishes. Bioacoustics 8, 185–208 (1997).
Yabe, M. Comparative osteology and myology of the superfamily Cottoidea (Pisces: Scorpaeniformes) and its phylogenetic classification. 32: 1–130. Mem. Fac. FIisheries, Hokkaido Univ. 32, 1–130 (1985).
Young, I. S. & Rome, L. C. Mutually exclusive muscle designs: the power output of the locomotory and sonic muscles of the oyster toadfish (Opsanus tau). Proc. R. Soc. London. Ser. B Biol. Sci. 268, 1965–1970 (2001).
Millot, S., Vandewalle, P. & Parmentier, E. Sound production in red-bellied piranhas (Pygocentrus nattereri, Kner): an acoustical, behavioural and morphofunctional study. J. Exp. Biol. 214, 3613–3618 (2011).
Tavolga, W. N. Review of marine bio-acoustics, state of the art (1964).
Fine, M. L., King, C. B. & Cameron, T. M. Acoustical properties of the swimbladder in the oyster toadfish Opsanus tau. J. Exp. Biol. 212, 3542–3552 (2009).
Fine, M. L., Bernard, B. & Harris, T. M. Functional morphology of toadfish sonic muscle fibers: relationship to possible fiber division. Can. J. Zool. 71, 2262–2274 (1993).
Boyle, K. S., Riepe, S., Bolen, G. & Parmentier, E. Variation in swim bladder drumming sounds from three doradid catfish species with similar sonic morphologies. J. Exp. Biol. 218, 2881–2891 (2015).
Boyle, K. S., Bolen, G. & Parmentier, E. Agonistic sounds and swim bladder morphology in a malapterurid electric catfish. J. Zool. 296, 249–260 (2015).
Rome, L. C., Syme, D. A., Hollingworth, S., Lindstedt, S. L. & Baylor, S. M. The whistle and the rattle: the design of sound producing muscles. Proc. Natl. Acad. Sci. USA 93, 8095–8100 (1996).
Feher, J., Waybright, T. & Fine, M. Comparison of sarcoplasmic reticulum capabilities in toadfish (Opsanus tau) sonic muscle and rat fast twitch muscle. J. Muscle Res. Cell Motil. 19, 661–674 (1998).
Ladich, F. & Myrberg, A. A. J. In Communication in fishes. (eds Ladich, F., Collin, S. P., Moller, P. & Kapoor, B. G.) 122–148 (Science Publishers, 2006).
Ladich, F. Agonistic behaviour and significance of sounds in vocalizing fish. Mar. Freshw. Behav. Physiol. 29, 87–108 (1997).
Bass, A. H. & Ladich, F. Vocal acoustic communication: from neurons to behaviour. In Fish Bioacoustics. (eds Popper, A. N., Fay, R. R. & Webb, J. F.) 253–278 (Springer, 2008).
Fine, M. L. & Waybright, T. D. Grunt variation in the oyster toadfish Opsanus tau: effect of size and sex. PeerJ 3, e1330 (2015).
Colleye, O., Frederich, B., Vandewalle, P., Casadevall, M. & Parmentier, E. Agonistic sounds in the skunk clownfish Amphiprion akallopisos: size-related variation in acoustic features. J. Fish Biol. 75, 908–916 (2009).
Connaughton, M. A., Taylor, M. H. & Fine, M. L. Effects of fish size and temperature on weakfish disturbance calls: implications for the mechanism of sound generation. J. Exp. Biol. 203, 1503–1512 (2000).
Mélotte, G., Vigouroux, R., Michel, C. & Parmentier, E. Interspecific variation of warning calls in piranhas: a comparative analysis. Sci. Rep. 6, 36127 (2016).
