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Comparative analysis of sound production between the bighead goby Ponticola kessleri and the round goby Neogobius melanostomus: Implications for phylogeny and systematics

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Abstract

Divergence in acoustic traits between closely related species can be explained by phylogenetic history. In gobies, phylogenies reconstructed with acoustic signals primarily overlap with studies based on morphological or molecular data. Here, sound production of the two Ponto-Caspian gobies, Neogobius melanostomus and Ponticola kessleri, was recorded in controlled conditions and compared to determine the degree of interspecific acoustic variation across benthophilin gobies. Both species produced tonal-like sounds characterized by unique temporal and spectral properties during agonistic and reproductive intraspecific interactions, while the acoustic comparison revealed that the vocalizations of these two species differ in almost every acoustic property. N. melanostomus vocal structure was characterised by short (c. 100 ms), low-frequency (< 100 Hz) tonal sounds repeated at a relatively faster rate, while P. kessleri sounds appeared as a broadband, downward frequency modulated longer calls (c. 450 ms). Some acoustic features (sound rate and duration) proved to be stereotyped and could be considered a species-specific trait that could potentially be utilized to discriminate males or used by females for mate assessment. The tonal sounds appear to have a deeper origin within the Benthophilinae subfamily, as all acoustically investigated species to date have been able to produce this sound type. The recorded vocal repertoire represents a baseline for future comparative acoustic studies among the benthophilin gobies, aiming to gain additional information on the evolution of acoustic communication within Ponto-Caspian gobies and highlighting their importance in reconstructing phylogenetic relationships.

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References

  • Agorreta A, San Mauro D, Schliewen U, Van Tassell JL, Kovačić M, Zardoya R, Ruber L (2013) Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Mol Phylogenet Evol 69:619–633

    Article  PubMed  Google Scholar 

  • Akamatsu A, Okumura T, Novarini N, Yan HY (2002) Empirical refinements applicable to the recording of fish sounds in small tanks. J Acoust Soc Am 112:3073–3082

    Article  PubMed  Google Scholar 

  • Amorim MCP (2006) Diversity of sound production in fish. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes, vol I. Science Publishers, Enfield, pp 71–105

    Google Scholar 

  • Amorim MCP, Neves ASM (2007) Acoustic signalling during courtship in the painted goby, Pomatoschistus pictus. J Mar Biol Assoc UK 87:1017–1023

    Article  Google Scholar 

  • Amorim MCP, Simões JM, Almada VC, Fonseca PJ (2011) Stereotypy and variation of the mating call in the Lusitanian toadfish, Halobatrachus didactylus. Behavioral Ecology and Sociobiology 65(4):707–716

  • Amorim MCP, Pedroso SS, Bolgan M, Jordão JM, Caiano M, Fonseca PJ (2013) Painted gobies sing their quality out loud: acoustic rather than visual signals advertise male quality and contribute to mating success. Funct Ecol 27:289–298. https://doi.org/10.1111/13652435.12032

    Article  Google Scholar 

  • Bass AH, Mckibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Neurobiology 605:1–26

    Google Scholar 

  • Berg LS (1949) Ryby presnykh vod SSSR i sopredel’nykh stran. Ch. 3 (freshwater fishes of the USSR and adjacent countries. Part 3, Moscow: Akad. Nauk SSSR

  • Bianco PG, Miller PJ (1990) Yugoslavian and other records of the Italian freshwater goby Padogobius martensii, and a character polarization in gobioid fishes. J Nat Hist 24:1289–1302. https://doi.org/10.1080/00222939000770761

    Article  Google Scholar 

  • Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Cap H, Deleporte P, Joachim J, Reby D (2008) Male vocal behavior and phylogeny in deer. Cladistics 24:917–931

    Article  PubMed  Google Scholar 

  • Christie PJ, Mennill DJ, Ratcliffe LM (2004) Chickadee song structure is individually distinctive over long broadcast distances. Behav 141:101–124

    Article  Google Scholar 

  • Cocroft RB, Ryan MJ (1995) Patterns of advertisement call evolution in toads and chorus frogs. Animal Behav 49:283–303

    Article  Google Scholar 

  • 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 Evol Biol 11:365

    Article  PubMed  PubMed Central  Google Scholar 

  • Crawford JD (1997) Hearing and acoustic communication in mormyrid electric fishes. Mar Freshw Behav Physiol 29:65–86

    Article  Google Scholar 

  • Gingras B, Mohandesan E, Boko D, Fitch WT (2013) Phylogenetic signal in the acoustic parameters of the advertisement calls of four clades of anurans. BMC Evol Biol 13:134. https://doi.org/10.1186/1471-2148-13-134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Günther AC (1861) Catalogue of Fishes in the British Museum 3:409–467

  • Hamao S, Sugit N, Nishiumi I (2015) Geographic variation in bird songs: examination of the effects of sympatric related species on the acoustic structure of songs. Acta Ethol 19:1–10. https://doi.org/10.1007/s10211-015-0228-6

    Article  Google Scholar 

  • Horvatić S, Cavraro F, Zanella D, Malavasi S (2015) Sound production in the Ponto-Caspian goby Neogobius fluviatilis and acoustic affinities within the Gobius lineage: implications for phylogeny. Biol J Linn Soc 117:564–573

    Article  Google Scholar 

  • Huyse T, Van Houdt J, Volckaert FAM (2004) Paleoclimatic history and vicariant speciation in the ‘sand goby’ group (Gobiidae, Teleostei). Mol Phylogenet Evol 32:324–336

    Article  CAS  PubMed  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kouelat, Comol, Switzerland and Freyhof. Berlin, Gennany

  • Kovačić M, Patzner RA (2011) North-Eastern Atlantic and Mediterranean gobius. In: Patzner RA, Van Tassell JL, Kovačić M, Kapoor BG (eds) The biology of gobies. Science Publishers, CRC Press, Taylor & Francis Group, New York, pp 177–206

    Google Scholar 

  • Kovačić M, Šanda R (2016) A new species of Gobius (Perciformes: Gobiidae) from the Mediterranean Sea and the redescription of Gobius bucchichi. J Fish Biol 88:1104–1124

    Article  PubMed  Google Scholar 

  • Ladich F, Kratochvil H (1989) Sound production in the marmoreal goby Proterorhinus marmoratus (Pallas) (Gobiidae: Teleostei). Zool Jahrb Abt allg Zool Physiol Tiere 93:501–504

    Google Scholar 

  • Laiolo P, Rolando A (2003) The evolution of vocalisations in the genus Corvus: effects of phylogeny, morphology and habitat. Evol Ecol 17:111–123

    Article  Google Scholar 

  • Lobel PS (1998) Possible species specific courtship sounds by two sympatric cichlids fishes in Lake Malati, Africa. Environ Biol Fish 52:443–452

    Article  Google Scholar 

  • Lugli M (2010) Sounds of shallow water fishes pitch within the quiet window of the habitat ambient noise. J Comp Physiol A 196:439–451. https://doi.org/10.1007/s00359-010-0528-2

    Article  Google Scholar 

  • Lugli M, Torricelli P (1999) Prespawning sound production in mediterranean sand gobies. J Fish Biol 54:691–694

    Article  Google Scholar 

  • Lugli M, Pavan G, Torricelli P, Bobbio L (1995) Spawning vocalisations in male freshwater gobiids (Pisces, Gobiidae). Environ Biol Fish 43:219–231

    Article  Google Scholar 

  • Lugli M, Torricelli P, Pavan G, Miller PJ (1996) Breeding sounds of male Padogobius nigricans with suggestions for further evolutionary study of vocal behaviour in gobioid fishes. J Fish Biol 49:648–657

    Google Scholar 

  • Lugli M, Torricelli P, Pavan G, Mainardi D (1997) Sound production during courtship and spawning among freshwater gobiids (Pisces, Gobiidae). Mar Fresh Behav Physiol 29:109–126

    Article  Google Scholar 

  • Lugli M, Yan HY, Fine ML (2003) Acoustic communication in two freshwater gobies: the relationship between ambient noise, hearing thresholds and sound spectrum. J Comp Physiol 189:309–320

    CAS  Google Scholar 

  • Malavasi S, Torricelli P, Lugli M, Pravoni F, Mainardi D (2003) Male courtship sounds in a teleost with alternative reproductive tactics, the grass goby, Zosterisessor ophiocephalus. Environ Biol Fish 66:231–236. https://doi.org/10.1023/A:1023923403180

    Article  Google Scholar 

  • Malavasi S, Collatuzzo S, Torricelli P (2008) Interspecific variation of acoustic signals in Mediterranean gobies (Perciformes, Gobiidae): comparative analysis and evolutionary outlook. Biol J Linn Soc 93:763–778. https://doi.org/10.1111/j.1095-8312.2008.00947.x

    Article  Google Scholar 

  • Malavasi S, Valerio C, Torricelli P (2009) Courtship sounds and associated behaviours in the Canestrini’s goby Pomatoschistus canestrinii. J Fish Biol 75:1883–1887

    Article  CAS  PubMed  Google Scholar 

  • Mann DA, Lobel PS (1995) Passive acoustic detection of sounds produced by the damselfish Dascyllus albisella (Pomacentridae). Bioacoustics 6:199–213

    Article  Google Scholar 

  • Medvedev DA, Sorokin PA, Vasil’ev VP, Chernova NV, Vasil’eva ED (2013) Reconstruction of phylogenetic relations of Ponto-Caspian gobies (Gobiidae, Perciformes) based on mitochondrial genome variation and some problems of their taxonomy. J Ichthyol 53:702–712

    Article  Google Scholar 

  • Mélotte G, Vigouroux R, Michel C, Parmentier E (2016) Interspecific variation of warning calls in piranhas: a comparative analysis. Sci Rep 6:36127. https://doi.org/10.1038/srep36127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller PJ (1984) The tokology of gobioid fishes. In: Potts GW, Wotton RJ (eds) Fish reproduction: strategies and tactics. Academic Press, London, pp 119–153

    Google Scholar 

  • Miller PJ (2003) The freshwater fishes of Europe. Mugilidae, Atherinidae, Atherinopsidae, Blenniidae, Odontobutidae, Gobiidae 1, Wiebelsheim: AULA Verlag, vol. 8/I, pp 157-345

  • Miller PJ (2004) The freshwater fishes of Europe. Gobiidae 2, Wiebelsheim: AULA Verlag, vol. 8/II, pp 33-93

  • Mitchell S, Poland J, Fine ML (2008) Does muscle fatigue limit advertisement calling in the oyster toadfish Opsanus tau? Animal Behav 76:1011–1016

    Article  Google Scholar 

  • Myrberg AA, Lugli M (2006) Reproductive behavior and acoustical interations. In: Ladich F, Collin SP, Moller P, Kaapor BG (eds) Communication in fishes, vol 1. Science Publishers, Enfield, pp 146–176

    Google Scholar 

  • Myrberg AA, Spanier E, Ha SJ (1978) Temporal patterning in acoustical communication. Contrasts in Behavior, Wiley, New York

    Google Scholar 

  • Neilson ME, Stepien CA (2009) Escape from the Ponto Caspian: evolution and biogeography of an endemic goby species flock (Benthophilinae: Gobiidae: Teleostei). Mol Phylogenet Evol 52:84–102

    Article  CAS  PubMed  Google Scholar 

  • Parmentier E, Kever L, Boyle K, Corbisier Y, Sawelew L, Malavasi S (2013) Sound production mechanism in Gobius paganellus (Gobiidae). J Exp Biol 216:3189–3199

    Article  PubMed  Google Scholar 

  • Penzo E, Gandolfi G, Bargelloni L, Colombo L, Patarnello T (1998) Messinian salinity crisis and the origin of freshwater lifestyle in western Mediterranean gobies. Mol Biol Evol 15:1472–1480

    Article  CAS  PubMed  Google Scholar 

  • Remage-Healey L, Bass AH (2006) A rapid, neuromodulatory role for steroid hormones in the control of reproductive behavior. Brain Res 1126:27–35

    Article  CAS  PubMed  Google Scholar 

  • Rice AN, Bass AH (2009) Novel vocal repertoire and paired swimbladders of the three-spined toadfish, Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae. J Exp Biol 212:1377–1391

    Article  PubMed  PubMed Central  Google Scholar 

  • Robillard T, Desutter-Grandcolas L (2004) High frequency calling in Eneopterinae crickets (Orthoptera, Grylloidea, Eneopteridae): adaptive radiation revealed by phylogenetic analysis. Biol J Linn Soc 83:577–584

    Article  Google Scholar 

  • Robillard T, Legendre F, Desutter-Grandcolas L, Grandcolas P (2006) Phylogenetic analysis and alignment of behavioral sequences by direct optimization. Cladistics 22:602–633

    Article  PubMed  Google Scholar 

  • Rollo A, Andraso G, Janssen J, Higgs D (2007) Attraction and localization of round goby (Neogobius melanostomus) to conspecific calls. Behaviour 144:1–21

    Article  Google Scholar 

  • Sebastianutto L, Picciulin M, Costantini M, Rocca M, Ferrero E (2008) Four types of sounds from one winner: vocalizations during territorial behaviour in the red-mouthed goby Gobius cruentatus (Pisces, Gobiidae). Acta Ethol 11:115–121

    Article  Google Scholar 

  • Simonovic PD, Nikolić VP, Skora KE (1996) Vertebral number in Ponto-Caspian gobies: phylogenetic relevance. J Fish Biol 49:1027–1029

    Article  Google Scholar 

  • Spanier E (1979) Aspects of species recognition by sound in four species of damselfishes, genus Eupomacentrus (Pisces: Pomacentridae). Z Tierpsychol 51:301–316. https://doi.org/10.1111/j.1439-0310.1979.tb00691.x

    Article  CAS  PubMed  Google Scholar 

  • Thacker CE (2011) Systematics of Gobiidae. In: Patzner RA, Van Tassell JL, Kovačić M, Kapoor BG (eds) The Biology of Gobies. Enfield, NH: Science Publishers, p 129–136

  • Thacker CE (2015) Biogeography of goby lineages (Gobiiformes: Gobioidei): origin, invasions, and extinction through the Cenozoic. J Biogeogr 42:1615–1625. https://doi.org/10.1111/jbi.12545

    Article  Google Scholar 

  • Thacker CE, Roje DM (2011) Phylogeny of Gobiidae and identification of gobiid lineages. Syst Biodivers 9:229–347

    Article  Google Scholar 

  • Thorson RF, Fine ML (2002) Crepuscular changes in emission rate and parameters of the boatwhistle advertisement call of the gulf toadfish, Opsanus beta. Environ Biol Fish 63:321–331. https://doi.org/10.1023/A:1014334425821

    Article  Google Scholar 

  • Torricelli P, Parmigiani S, Lugli M, Gandolfi G (1988) Intermale aggression in Padogobius martensi (günther) (pisces Gobiidae): effect of size and prior residence. Monit Zoolog Ital – Ital J Zool 22:121–131. https://doi.org/10.1080/00269786.1988.10736547

    Article  Google Scholar 

  • Torricelli P, Lugli M, Pavan G (1990) Analysis of sound produced by male Padogobius martensi (Pisces: Gobiidae) and factors affecting their structural properties. Bioacoustics 2:261–175

    Article  Google Scholar 

  • Zeyl JN, Malavasi S, Holt DE, Noel P, Lugli M, Johnston CE (2016) Convergent aspects of acoustic communication in darters, sculpins and gobies. In: Sisneros AJ (ed) Fish hearing and bioacoustics: an anthology in honor of Arthur N. Popper and Richard R. Fay. Springer International Publishing, Cham, pp 93–120

    Chapter  Google Scholar 

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Acknowledgements

Authors are grateful to Linda Zanella for proofreading the manuscript and two anonymous referees for their comments that improved the overall quality of the manuscript. All methods and procedures were approved by the Ethics Committee of Biology Division (Faculty of Science, approval no: 251-58-10617-18-14).

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  1. Department of Zoology, Faculty of Science, University of Zagreb, Rooseveltov trg 6, 10000, Zagreb, Croatia

    Sven Horvatić, Lea Bem, Zoran Marčić, Ivana Buj, Perica Mustafić & Davor Zanella

  2. Department Environmental Sciences, Informatics and Statistics, Ca` Foscari University of Venice, Via Torino 155, 30172, Venezia Mestre, Italy

    Stefano Malavasi

  3. Faculty of Teacher Education, University of Zagreb, Savska cesta 77, 10000, Zagreb, Croatia

    Marko Ćaleta

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  1. Sven Horvatić
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Horvatić, S., Bem, L., Malavasi, S. et al. Comparative analysis of sound production between the bighead goby Ponticola kessleri and the round goby Neogobius melanostomus: Implications for phylogeny and systematics. Environ Biol Fish 102, 727–739 (2019). https://doi.org/10.1007/s10641-019-00866-7

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