Characteristics of sound production and associated pharyngeal jaws in the tomtate grunt Haemulon aurolineatum (Cuvier, 1830) in Caribbean reefs

Morgane Millot, Frédéric Bertucci, David Lecchini , Sarah Smeets, Malika René-Trouillefou, Eric Parmentier

Abstract


The ability to produce sounds for acoustic communication is well known in different grunt species (Haemulidae). However, most of the sounds have not been described and the sound-producing mechanism of very few grunt species has been deeply studied. Additional data is needed to search for synapomorphy in the sonic mechanism. This study describes acoustic features and branchial anatomy in Haemulon aurolineatum. Correlations were found between some acoustic features and standard length, showing the largest specimens produced shorter, lower-pitched grunts of higher intensity. Examinations of acoustic features and branchial anatomy show that H. aurolineatum uses the same stridulatory mechanism described previously in H. flavolineatum. The unusual feature of Haemulon species concerns the fourth ceratobranchials. These appear to be part of the lower pharyngeal jaws since they possess firmly attached teeth that face the upper pharyngeal jaws. The stridulation results from the rubbing of both pharyngeal and fourth ceratobranchial teeth. This mechanism is probably common to the 23 Haemulon species, but additional information is needed regarding the mechanism of other Haemulinae species to produce stridulatory sounds. Fourth ceratobranchials could constitute a key element of Haemulinae ability to produce sounds providing an eventual synapomorphic aspect of the mechanism in the family.

Keywords


acoustic communication; pharyngeal jaws; stridulatory mechanism

Full Text:

PDF

References


Amorim M.C.P., Conti C., Modesto T., Gonçales A. & Fonseca P.J. (2015). Agonistic sounds signal male quality in the Lusitanian toadfish. Physiology & Behavior 149: 192–198. https://doi.org/10.1016/j.physbeh.2015.06.002

Amorim, M.C.P., Fonseca, P.J. & Almada V.C. (2003). Sound production during courtship and spawning of Oreochromis mossambicus: male–female and male–male interactions. Journal of Fish Biology 62: 658–672. https://doi.org/10.1046/j.1095-8649.2003.00054.x

Amorim M.C.P. & Hawkins A.D. (2005). Ontogeny of acoustic and feeding behaviour in the grey gurnard, Eutrigla gurnardus. Ethology 111: 255–269. https://doi.org/10.1111/j.1439-0310.2004.01061.x

Bertucci F., Attia J., Beauchaud M. & Mathevon N. (2012). Sounds produced by the cichlid fish Metriaclima zebra allow reliable estimation of size and provide information on individual identity. Journal of Fish Biology 80: 752–766. https://doi.org/10.1111/j.1095-8649.2012.03222.x

Bertucci F., Ruppé L., Van Wassenbergh S., Compère P. & Parmentier E. (2014). New insights into the role of the pharyngeal jaw apparatus in the sound-producing mechanism of Haemulon flavolineatum (Haemulidae). Journal of Experimental Biology 217: 3862–3869. Available from https://jeb.biologists.org/content/217/21/3862 [accessed 12 February 2021].

Boyle K.S. & Tricas T.C. (2011). Sound production in the longnose butterflyfishes (genus Forcipiger): cranial kinematics, muscle activity and honest signals. Journal of Experimental Biology 214: 3829–3842. Available from https://jeb.biologists.org/content/214/22/3829 [accessed 12 February 2021].

Burkenroad M.D. (1930). Sound production in the Haemulidae. Copeia 1930: 17–18.

Colleye O., Frédérich B., Vandewalle P., Casadevall M. & Parmentier E. (2009). Agonistic sounds in the skunk clownfish Amphiprion akallopisos: size related variation in acoustic features. Journal of Fish Biology 75: 908–916. https://doi.org/10.1111/j.1095-8649.2009.02316.x

Colleye O., Vandewalle P., Lanterbecq D., Lecchini D. & Parmentier E. (2011). Interspecific variation of calls in clownfishes: degree of similarity in closely related species. BMC evolutionary biology 11: 365. https://doi.org/10.1186/1471-2148-11-365

Colleye O & Parmentier E (2012). Overview on the diversity of sounds produced by clownfishes (Pomacentridae): importance of acoustic signals in their peculiar way of life. PLoS ONE 7 (11): e49179. https://doi.org/10.1371/journal.pone.0049179

Connaughton M.A., Taylor M.H. & Fine M.L. (2000). Effects of fish size and temperature on weakfish disturbance calls: implications for the mechanism of sound generation. Journal of Experimental Biology 203: 1503–1512.

Cummings W.C., Brahy B.D. & Spires J.Y. (1966). Sound production, schooling, and feeding habits of the margate, Haemulon album Cuvier, off North Bimini, Bahamas. Bulletin of Marine Science 16: 626–640.

Darcy, G.H. 1983. Synopsis of biological data on the grunts Haemulon aurolineatum and H. plumieri (Pisces: Haemulidae). FAO Fisheries Synopsis 133.

De Jong K., Bouton N. & Slabbekoorn H. (2007). Azorean rock-pool blennies produce size-dependent calls in a courtship context. Animal Behaviour 74: 1285–1292. https://doi.org/10.1016/j.anbehav.2007.02.023

Demski L.S., Gerald J.W. & Popper A.N. (1973). Central and peripheral mechanisms of teleost sound production. American Zoologist 13: 1141–1167.

Fine M.L., McElroy D., Rafi J., King C.B., Loesser K.E. & Newton S. (1996). Lateralization of pectoral stridulation sound production in the channel catfish. Physiology & Behavior 60: 753–757. https://doi.org/10.1016/0031-9384(96)00092-3

Fine M.L. & Parmentier E. (2015). Mechanisms of fish sound production. In: Ladich F. (ed.) Sound Communication in Fishes: 77–126. Springer, Wien.

Fish M.P. & Mowbray W.H. (1970). Sounds of Western North Atlantic Fishes: A Reference File of Biological Underwater Sounds. The Johns Hopkins University Press, Baltimore.

Fishbase. (2019). Scientific names where genus equals haemulon. Available from www.fishbase.org [accessed July 2020].

Gerald J.W. (1971). Sound production during courtship in six species of sunfish (Centrarchidae). Evolution 25: 75–87. Available from https://www.jstor.org/stable/2406500 [accessed 12 February 2021].

Gould S.J. & Vrba E.S. (1982). Exaptation: a missing term in the science of form. Paleobiology 8: 4–15. Available from https://www.jstor.org/stable/2400563 [accessed 12 February 2021].

Hawkins A.D. & Rasmussen K.J. (1978). The calls of gadoid fish. Journal of the Marine Biological Association of the United Kingdom 58: 891–911. https://doi.org/10.1017/S0025315400056848

Henglmüller S.M. & Ladich F. (1999). Development of agonistic behaviour and vocalization in croaking gouramis. Journal of Fish Biology 54: 380–395. https://doi.org/10.1111/j.1095-8649.1999.tb00837.x

Johnson G.D. (1981). The limits and relationships of the Lutjanidae and associated families. In: Cox C.S., Vincent E.S., Flem-Inger A. & Rosenblatt R.H. (eds) Bulletin of the Scripps Institution of Oceanography: 1–112. University of California Press, Berkeley.

Knight L. & Ladich F. (2014). Distress sounds of thorny catfishes emitted underwater and in air: characteristics and potential significance. Journal of Experimental Biology 217: 4068–4078. https://doi.org/10.1242/jeb.110957

Lim A.C.O., Chong V.C., Chew W.X., Muniandy S.V., Wong C.S. & Ong Z.C. (2015). Sound production in the tiger-tail seahorse Hippocampus comes: insights into the sound producing mechanisms. The Journal of the Acoustical Society of America 138: 404–412. https://doi.org/10.1121/1.4923153

Lindström K. & Lugli M. (2000). A quantitative analysis of the courtship acoustic behaviour and sound patterning in male sand goby, Pomatoschistus minutus. Environmental Biology of Fishes 58: 411–424. https://doi.org/10.1023/A:1007695526177

Lobel P.S. (1992). Sounds produced by spawning fishes. Environmental Biology of Fishes 33: 351–358. https://doi.org/10.1007/BF00010947

Lobel P.S. & Mann D.A. (1995). Spawning sounds of the damselfish, Dascyllus albisella (Pomacentridae), and relationship to male size. Bioacoustics 6: 187–198. https://doi.org/10.1080/09524622.1995.9753289

Malavasi S., Collatuzzo S. & Torricelli P. (2008). Interspecific variation of acoustic signals in Mediterranean gobies (Perciformes, Gobiidae): comparative analysis and evolutionary outlook. Biological Journal of the Linnean Society 93: 763–778. https://doi.org/10.1111/j.1095-8312.2008.00947.x

Manooch C.S. & Barans C.A. (1982). Distribution, abundance, and age and growth of the tomtate, Haemulon aurolineatum, along the southeastern United States coast. Fishery Bulletin 80: 1–20.

Moulton J.M. (1958). The acoustical behavior of some fishes in the Bimini area. The Biological Bulletin 114: 357–374. https://doi.org/10.2307/1538991

Myrberg A.A. & Lugli M. (2006). Reproductive behavior and acoustical interactions. In: Ladich F., Collin S.P., Moller P. & Kapoor B.G. (eds) Communication in Fishes: 149–176. Science Publishers Inc., Enfield.

Myrberg Jr A.A., Ha S.J. & Shamblott M.J. (1993). The sounds of bicolor damselfish (Pomacentrus partitus): predictors of body size and a spectral basis for individual recognition and assessment. The Journal of the Acoustical Society of America 94: 3067–3070. https://doi.org/10.1121/1.407267

Parmentier E., Fabri G., Kaatz I., Decloux N., Planes S. & Vandewalle P. (2010a). Functional study of the pectoral spine stridulation mechanism in different mochokid catfishes. Journal of Experimental Biology 213: 1107–1114. https://doi.org/10.1242/jeb.039461

Parmentier E., Kéver L., Casadevall M. & Lecchini D. (2010b). Diversity and complexity in the acoustic behaviour of Dacyllus flavicaudus (Pomacentridae). Marine Biology 157: 2317–2327. https://doi.org/10.1007/s00227-010-1498-1

Parmentier E., Kéver L., Boyle K., Corbisier, Y.-E., Sawelew L. & Malavasi S. (2013). Sound production mechanism in Gobius paganellus (Gobiidae). Journal of Experimental Biology 216: 3189–3199. https://doi.org/10.1242/jeb.087205

Parmentier E., Tock J., Falguière J.-C. & Beauchaud M. (2014). Sound production in Sciaenops ocellatus: preliminary study for the development of acoustic cues in aquaculture. Aquaculture 432: 204–211. https://doi.org/10.1016/j.aquaculture.2014.05.017

Parmentier E. & Fine M.L. (2016). Fish sound production: insights. In: Suthers R.A., Tecumseh F., Fay R.R. & Popper A.N. (eds) Vertebrate Sound Production and Acoustic Communication: 19–46. Springer, Handbook of Auditory Research vol. 53. https://doi.org/10.1007/978-3-319-27721-9_2

Parmentier E., Diogo R. & Fine M.L. (2017a). Multiple exaptations leading to fish sound production. Fish and Fisheries 18: 958–966. https://doi.org/10.1111/faf.12217

Parmentier E., Raick X., Lecchini D., Boyle K., Van Wassenbergh., Bertucci F. & Kéver L. (2017b). Unusual sound production mechanism in the triggerfish Rhinecanthus aculeatus (Balistidae). Journal of Experimental Biology 220: 186–193. https://doi.org/10.1242/jeb.157263

Parmentier E., Kéver L., Boyle K., Corbisier, Y.-E., Sawelew L. & Malavasi S. (2013). Sound production mechanism in Gobius paganellus (Gobiidae). Journal of Experimental Biology 216: 3189–3199. https://doi.org/10.1242/jeb.087205

Parmentier E., Tock J., Falguière J.-C. & Beauchaud M. (2014). Sound production in Sciaenops ocellatus: preliminary study for the development of acoustic cues in aquaculture. Aquaculture 432: 204–211. https://doi.org/10.1016/j.aquaculture.2014.05.017

Pedroso S.S., Barber I., Svensson O., Fonseca P.J. & Amorim M.C.P. (2013). Courtship sounds advertise species identity and male quality in sympatric Pomatoschistus spp. gobies. PLoS One 8: e64620. https://doi.org/10.1371/journal.pone.0064620

Picciulin M., Sebastianutto L., Costantini M., Rocca M. & Ferrero E.A. (2006). Aggressive territorial ethogram of the red-mouthed goby, Gobius cruentatus (Gmelin, 1789). Electronic Journal of Ichthyology 2: 8419.

Pruzsinszky I. & Ladich F. (1998). Sound production and reproductive behaviour of the armoured catfish Corydoras paleatus (Callichthyidae). Environmental Biology of Fishes 53: 183–191. https://doi.org/10.1023/A:1007413108550

RCore Team (2018). R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

Schneider H. (1967). Morphology and physiology of sound-producing mechanisms in teleost fishes. Marine Bio-Acoustics 2: 135–158.

Takemura A. (1984). Acoustical behavior of the freshwater goby Odontobutis obscura. Bulletin of the Japanese Society of Scientific Fisheries 50: 561–564.

Tavolga W.N. (1971). Sound production and detection. Fish physiology. In: Hoar W.S. & Randall D.J. (eds) Fish Physiology, vol. 5: 135–205. Academic press, New York.

Tavolga W.N. & Wodinsky J. (1965). Auditory capacities in fishes: threshold variability in the blue-striped grunt, Haemulon sciurus. Animal Behaviour 13: 301–311. https://doi.org/10.1016/0003-3472(65)90050-3

Tellechea J.S., Martinez C., Fine M.L. & Norbis W. (2010). Sound production in the whitemouth croaker and relationship between fish size and disturbance call characteristics. Environmental Biology of Fishes 89: 163–172. https://doi.org/10.1007/s10641-010-9709-7

Vandewalle P., Parmentier E. & Chardon M. (2000). The branchial basket in Teleost feeding. Cybium 24: 319-342.

Wainwright P.C. (1989a). Functional morphology of the pharyngeal jaw apparatus in perciform fishes: an experimental analysis of the Haemulidae. Journal of Morphology 200: 231–245. https://doi.org/10.1002/jmor.1052000302

Wainwright P.C. (1989b). Prey processing in haemulid fishes: patterns of variation in pharyngeal jaw muscle activity. Journal of Experimental Biology 141: 359–375.

Wainwright P.C. (2005). Functional morphology of the pharyngeal jaw apparatus. Fish physiology 23: 77–101. https://doi.org/10.1016/S1546-5098(05)23003-0




DOI: https://doi.org/10.26496/bjz.2021.84

Refbacks

  • There are currently no refbacks.


The Royal Belgian Society of Zoology acknowledges the Universitarian Foundation of Belgium and the National Fund of Scientific Research for their financial support in publishing the Belgian Journal of Zoology.