[en] The Neretva dwarf goby Orsinigobius croaticus (Gobiiformes, Gobionellidae) is an endemic fish native to the freshwaters of the Adriatic Basin in Croatia and Bosnia and Herzegovina, a Mediterranean Biodiversity Hotspot. Due to its limited distribution range, specific karst habitat and endangered status, laboratory studies on reproductive biology are scarce but crucial. Herein, we investigated the sound production and acoustic behaviour of the endangered O. croaticus during reproductive intersexual laboratory encounters, utilising an interdisciplinary approach. We also performed dissections and micro-computed tomography (μCT) scanning of the pectoral girdle to explore its potential involvement in sound production. Finally, comparative acoustic analysis was conducted on sounds produced by previously recorded soniferous sand gobies to investigate whether acoustic features are species-specific. The endemic O. croaticus is a soniferous species. Males of this species emit pulsatile sounds composed of a variable number of short (~15 ms) consecutive pulses when interacting with females, usually during the pre-spawning phase in the nest, but also during courtship outside the nest. Pulsatile sounds were low-frequency and short pulse trains (~140 Hz, <1000 ms). Male visual behaviour rate was higher when co-occurring with sounds and females entered the male's nest significantly more frequently when sounds were present. Characteristic body movements accompanied male sound production, such as head thrust and fin spreading. Furthermore, μCT scans and dissections suggest that O. croaticus shares certain anatomical similarities of the pectoral girdle (i.e. osseous elements and arrangement of levator pectoralis muscles) to previously studied sand gobies that could be involved in sound production. Multivariate comparisons, using sounds produced by eight soniferous European sand gobies, effectively distinguished soniferous (and sympatric) species based on their acoustic properties. However, the discrimination success decreased when temperature-dependent features (sound duration and pulse repetition rate) were excluded from the analysis. Therefore, we suggest both spectral and temporal features are important for the acoustic differentiation of sand gobies.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège [BE] AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Horvatić, Sven; Department of Zoology, Faculty of Science, University of Zagreb, Zagreb, Croatia
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Malavasi, Stefano; Department of Environmental Sciences, Informatics and Statistics, Cà Foscari, University of Venice, Italy
Amorim, Maria; Departamento de Biologia Animal and MARE -Marine and Environmental Sciences Centre, Faculdade de Ciências, ARNET -Aquatic Research Network, Universidade de Lisboa, Lisbon, Portugal
Fonseca, Paulo; cE3c -Centre for Ecology, Evolution and Environmental Changes, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Zanella, Davor; Department of Zoology, Faculty of Science, University of Zagreb, Zagreb, Croatia
Language :
English
Title :
Endemic fish calling: Acoustics and reproductive behaviour of the Neretva dwarf goby Orsinigobius croaticus
Abell, R., Thieme, M. L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras Balderas, S., Bussing, W., Stiassny, M. L. J., Skelton, P., Allen, G. R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., … Petry, P. (2008). Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 58(5), 403–414. https://doi.org/10.1641/B580507
Abramoff, M. D., Magalhaes, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11(7), 36–42.
Adriaens, D., Decleyre, D., & Verraes, W. (1993). Morphology of the pectoral girdle in Pomatoschistus lozanoi De Buen, 1923 (Gobiidae), in relation to pectoral fin adduction. Belgian Journal of Zoology, 123, 137–157.
Agorreta, A., San Mauro, D., Schliewen, U. K., Van Tassell, J. L., Kovačić, M., Zardoya, R., & Rüber, L. (2013). Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies. Molecular Phylogenetics and Evolution, 69(3), 619–633. https://doi.org/10.1016/j.ympev.2013.07.013
Akamatsu, A., Okumura, T., Novarini, N., & Yan, H. Y. (2002). Empirical refinements applicable to the recording of fish sounds in small tanks. Journal of the Acoustical Society of America, 112, 3073–3082. https://doi.org/10.1121/1.1518218
Amorim, M. C. P. (2006). Diversity of sound production in fish. In F. Ladich (Ed.), Communication in fishes, vol. 1 (pp. 71–105). Science Publishers.
Amorim, M. C. P., & Neves, A. S. M. (2007). Acoustic signalling during courtship in the painted goby, Pomatoschistus pictus. Journal of the Marine Biological Association of the United Kingdom, 87, 1017–1023. https://doi.org/10.1017/S0025315407056822
Amorim, M. C. P., & Neves, A. S. M. (2008). Male painted goby (Pomatoschistus pictus) vocalize to defend territories. Behaviour, 145, 1065–1083.
Amorim, M. C. P., Pedroso, S. S., Bolgan, M., Jordão, J. M., Caiano, M., & Fonseca, P. J. (2013). Painted gobies sing their quality out loud: Acoustic rather than visual signals advertise male quality and contribute to mating success. Functional Ecology, 27, 289–298. https://doi.org/10.1111/1365-2435.12032
Amorim, M. C. P., Simões, J. M., Fonseca, P. J., & Turner, G. F. (2008). Species differences in courtship acoustic signals among five Lake Malawi cichlid species (Pseudotropheus spp.). Journal of Fish Biology, 72, 1355–1368.
Amorim, M. C. P., Simões, J. M., Mendonça, N., Bandarra, N. M., Almada, V. C., & Fonseca, P. J. (2010). Lusitanian toadfish song reflects male quality. Journal of Experimental Biology, 213(17), 2997–3004. https://doi.org/10.1242/jeb.041020
Amorim, M. C. P., Vasconcelos, R. O., Bolgan, M., Pedroso, S. S., & Fonseca, P. J. (2018). Acoustic communication in marine shallow waters: Testing the acoustic adaptive hypothesis in sand gobies. Journal of Experimental Biology, 221(Pt 22), jeb183681. https://doi.org/10.1242/jeb.183681
Bennett, A. F. (1985). Temperature and muscle. Journal of Experimental Biology, 115, 333–344.
Bertucci, F., Parmentier, E., Hillion, A., Cordonnier, S., Lecchini, D., & René-Trouillefou, M. (2021). First highlight of sound production in the glassy sweeper Pempheris schomburgkii (Pempheridae). Marine Biology, 168(32). https://doi.org/10.1007/s00227-021-03829-8
Betancur-R, R., Wiley, E. O., Arratia, G., Acero, A., Bailly, N., Miya, M., Lecointre, G., & Ortí, G. (2017). Phylogenetic classification of bony fishes. BMC Evolutionary Biology, 17(1), 162. https://doi.org/10.1186/s12862-017-0958-3
Blom, E. L., Mück, I., Heubel, K., Müller, R., Schulz-Mirbach, T., & Ladich, F. (2016). Acoustic and visual courtship traits in two sympatric marine Gobiidae species – Pomatoschistus microps and Pomatoschistus minutus. Environmental Biology of Fishes, 99, 999–1007. https://doi.org/10.1007/s10641-016-0550-5
Bolgan, M., Crucianelli, A., Mylonas, C. C., Henry, S., Falguière, J. C., & Parmentier, E. (2020). Calling activity and calls' temporal features inform about fish reproductive condition and spawning in three cultured Sciaenidae species. Aquaculture, 524, 735243.
Bolgan, M., Pedroso, S. S., Picciulin, M., Fonseca, P. J., & Amorim, M. C. P. (2013). Differential investment in acoustic communication during social interactions in two closely-related sand goby species. Behaviour, 150(2), 133–152. https://doi.org/10.1163/1568539X-00003041
Bro-Jørgensen, J. (2010). Dynamics of multiple signalling systems: Animal communication in a world in flux. Trends in Ecology & Evolution, 25, 292–300.
Ćaleta, M., Buj, I., Mrakovčić, M., Mustafić, P., Zanella, D., Marčić, Z., Duplić, A., Mihinjač, T., & Katavić, I. (2015). Endemic fish of Croatia. Agencija Za zaštitu okoliša, 116 pp. (in Croatian).
Ćaleta, M., Marčić, Z., Buj, I., Zanella, D., Mustafić, P., Duplić, A., & Horvatić, S. (2019). A review of extant Croatian freshwater fish and lampreys. Annotated list and distribution. Croatian Journal of Fisheries, 77(3), 136–232. https://doi.org/10.2478/cjf-2019-0016
Chang, H. J., Mok, H. K., Fine, M. L., Soong, K., Chen, Y. Y., & Chen, T. Y. (2022). Vocal repertoire and sound characteristics in the variegated cardinalfish, Fowleria variegata (Pisces: Apogonidae). The Journal of the Acoustical Society of America, 152(6), 3716–3727. https://doi.org/10.1121/10.0016441
Crivelli, A. J. (2018). Orsinigobius croatica (amended version of 2006 assessment). The IUCN red list of threatened species 2018: E.T11031A136231892. https://doi.org/10.2305/IUCN.UK.2006.RLTS.T11031A136231892.en
Darwall, W., Carrizo, S., Numa, C., Barrios, V., Freyhof, J., & Smith, K. (2014). Freshwater key biodiversity areas in the Mediterranean Basin hotspot: Informing species conservation and development planning in freshwater ecosystems. IUCN. x + 86 pp.
de Jong, K., Amorim, M. C. P., Fonseca, P. J., Fox, C. J., & Heubel, K. U. (2017). Noise can affect acoustic communication and subsequent spawning success in fish. Environmental Pollution, 237, 814–823. https://doi.org/10.1016/j.envpol.2017.11.003
de Jong, K., Amorim, M. C. P., Fonseca, P. J., Klein, A., & Heubel, K. U. (2016). Noise affects acoustic courtship behavior similarly in two species of gobies. Proceedings of Meetings on Acoustics, 27, 010018 https://doi.org/10.1121/2.0000272
Erisman, B. E., & Rowell, T. J. (2017). A sound worth saving: Acoustic characteristics of a massive fish spawning aggregation. Biology Letters, 13, 20170656. https://doi.org/10.1098/rsbl.2017.0656
Fine, M. L., & Parmentier, E. (2015). Mechanisms of fish sound production. In F. Ladich (Ed.), Sound communication in fishes (animal signals and communication, vol. 4, pp. 39–62). Springer Vienna. https://doi.org/10.1007/978-3-7091-1846-7_3
Freyhof, J. (2011). Diversity and distribution of freshwater gobies from the Mediterranean, the black and Caspian seas. In R. A. Patzner, J. L. van Tassell, M. Kovačić, & B. G. Kapoor (Eds.), The biology of gobies (pp. 279–288). Science Publishers, CRC Press.
Gkenas, C., Malavasi, S., Georgalas, V., Leonardos, I. D., & Torricelli, P. (2010). The reproductive behaviour of Economidichthys pygmaeus: Secondary loss of sound production within the sand goby group? Environmental Biology of Fishes, 87, 299–307. https://doi.org/10.1007/s10641-010-9597-x
Hawkins, A. D., & Amorim, M. C. P. (2000). Spawning sounds of the male haddock, Melanogrammus aeglefinus. Environmental Biology of Fishes, 59, 29–41.
Heuschele, J., Mannerla, M., Gienapp, P., & Candolin, U. (2009). Environment-dependent use of mate choice cues in sticklebacks. Behavioral Ecology, 20(6), 1223–1227. https://doi.org/10.1093/beheco/arp123
Horvatić, S., Cavraro, F., Zanella, D., & Malavasi, S. (2016). Sound production in the Ponto-Caspian goby Neogobius fluviatilis and acoustic affinities within the Gobius lineage: Implications for phylogeny. Biological Journal of the Linnean Society, 117(3), 564–573.
Horvatić, S., Malavasi, S., Vukić, J., Šanda, R., Marčić, Z., Ćaleta, M., Lorenzoni, M., Mustafić, P., Ivana Buj, I., Lucija Onorato, L., Lucija Ivić, L., Francesco Cavraro, F., & Zanella, D. (2021). Correlation between acoustic divergence and phylogenetic distance in soniferous European gobiids (Gobiidae; Gobius lineage). PLoS One, 16(12), e0260810. https://doi.org/10.1371/journal.pone.0260810
Horvatić, S., Marčić, Z., Mrakovčić, M., Mustafić, P., Buj, I., Ćaleta, M., & Zanella, D. (2017). Threatened fishes of the world: Orsinogobius croaticus (Mrakovčić, Kerovec, Mišetić & Schneider, 1996) (Teleostei: Gobiidae). Croatian Journal of Fisheries, 75, 30–35.
Jublier, N., Bertucci, F., Kéver, L., Colleye, O., Ballesta, L., Nemeth, R. S., Lecchini, D., Rhodes, K. L., & Parmentier, E. (2019). Passive monitoring of phenological acoustic patterns reveals the sound of the camouflage grouper, epinephelus polyphekadion. Aquatic Conservation: Marine and Freshwater Ecosystems, 30, 42–52. https://doi.org/10.1002/aqc.3242
Knapp, R. A., & Kovach, J. T. (1991). Courtship as an honest indicator of male parental quality in the bicolor damselfish, Stegastes partitus. Behavioral Ecology, 2, 230–295. https://doi.org/10.1093/beheco/2.3.230
Kottelat, M., & Freyhof, J. (2007). Handbook of European freshwater fishes. Freyhof.
Kovačić, M. (2008). The key for identification of Gobiidae (Pisces: Perciformes) in the Adriatic Sea. Acta Adriatica, 49, 245–254.
Kovačić, M., & Patzner, R. A. (2011). North-eastern Atlantic and Mediterranean gobies. In R. A. Patzner, J. L. van Tassell, M. Kovačić, & B. G. Kapoor (Eds.), The biology of gobies (pp. 177–193). Science Publishers, CRC Press.
Kutle, A. (Ed.). (1999). Pregled stanja biološke i krajobrazne raznolikosti Hrvatske sa strategijom i akcijskim planovima zaštite [review of the state of biological and landscape diversity of Croatia with strategy and action plans for protection]. Državna uprava za zaštitu prirode i okoliša.
Ladich, F. (2018). Acoustic communication in fishes: Temperature plays a role. Fish and Fisheries, 19(4), 598–612. https://doi.org/10.1111/faf.12272
Ladich, F., & Kratochvil, H. (1989). Sound production in the marmoreal goby Proterorhinus marmoratus (Pallas) (Gobiidae:Teleostei). Zoologische Jahrbücher Abteilung für Allgemeine Zoologie Und Physiologie der Tiere, 93, 501–504.
Levine, J. S., Lobel, P. S., & MacNichol, E. F. (1980). Visual communication in fishes. In M. A. Ali (Ed.), Environmental physiology of fishes. NATO advanced study institutes series, vol 35. Springer. https://doi.org/10.1007/978-1-4899-3659-2_17
Liley, N. R. (1982). Chemical communication in fish. Canadian Journal of Fisheries and Aquatic Sciences, 39, 22–35.
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(4), 411–424. https://doi.org/10.1023/A:1007695526177
Lobel, P. (1992). Sounds produced by spawning fishes. Environmental Biology of Fishes, 33, 351–358. https://doi.org/10.1007/bf00010947
Lobel, P. S. (2001). Acoustic behavior of cichlid fishes. Journal of Aquariculture and Aquatic Sciences, 9, 167–186.
Lobel, P. S. (2002). Diversity of fish spawning sounds and the application of passive acoustic monitoring. Bioacoustics, 12, 286–289. https://doi.org/10.1080/09524622.2002.9753724
Lombarte, A., Miletić, M., Kovačić, M., Otero-Ferrer, J. L., & Tuset, V. M. (2018). Identifying sagittal otoliths of Mediterranean Sea gobies: Variability among phylogenetic lineages. Journal of Fish Biology, 92, 1768–1787. https://doi.org/10.1111/jfb.13615
Longrie, N., Poncin, P., Denoël, M., Gennotte, V., Delcourt, J., & Parmentier, E. (2013). Behaviours associated with acoustic communication in Nile tilapia (Oreochromis niloticus). PLoS One, 8, e61467. https://doi.org/10.1371/journal.pone.0061467
Lugli, M., Pavan, G., Torricelli, P., & Bobbio, L. (1995). Spawning vocalizations in male freshwater gobiids (Pisces, Gobiidae). Environmental Biology of Fishes, 43, 219–231. https://doi.org/10.1007/BF00005853
Lugli, M., & Torricelli, P. (1999). Prespawning sound production in Mediterranean sand-gobies. Journal of Fish Biology, 54, 691–694.
Lugli, M., Torricelli, P., Pavan, G., & Mainardi, D. (1997). Sound production during courtship and spawning among freshwater gobiids (Pisces, Gobiidae). Marine and Freshwater Behaviour and Physiology, 29, 109–126. https://doi.org/10.1080/10236249709379003
Lugli, M., Torricelli, P., Pavan, G., & Miller, P. J. (1996). Breeding sounds of male Padogobius nigricans with suggestions for further evolutionary study of vocal behaviour in gobioid fishes. Journal of Fish Biology, 49(4), 648–657.
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
Malavasi, S., Gkenas, C., Leonardos, I., Torricelli, P., & McLennan, D. A. (2012). The phylogeny of a reduced ‘sand goby’ group based on behavioural and life history characters. Zoological Journal of the Linnean Society, 165(4), 916–924. https://doi.org/10.1111/j.1096-3642.2012.00832.x
Malavasi, S., Valerio, C., & Torricelli, P. (2009). Courtship sounds and associated behaviours in the Canestrini's goby Pomatoschistus canestrinii. Journal of Fish Biology, 75, 1883–1887.
Mann, D. A., Hawkins, A. D., & Jech, J. M. (2008). Active and passive acoustics to locate and study fish. In J. F. Webb, R. R. Fay, & A. N. Popper (Eds.), Fish bioacoustics (Springer handbook of auditory research, vol. 32, pp. 301–327. Springer. https://doi.org/10.1007/978-0-387-73029-5_9
Mazzoldi, C., & Rassotto, M. B. (2001). Extended breeding season in the marbled goby Pomatoschistus marmoratus (Teleostei: Gobiidae), in the venetian lagoon. Environmental Biology of Fishes, 61(2), 175–183. https://doi.org/10.1023/A:1011030408898
Melotte, G., Vigouroux, R., Michel, C., & Parmentier, E. (2016). Interspecific variation of warning calls in piranhas: A comparative analysis. Scientific Reports, 6, 3612. https://doi.org/10.1038/srep36127
Miller, P. J. (1986). Gobiidae. In P. J. P. Whitehead, M. L. Bauchot, J. C. Hureau, J. Nielsen, & E. Tortonese (Eds.), Fishes of the North-Eastern Atlantic and the Mediterranean, volume 3 (pp. 1019–1085). UNESCO.
Miller, P. J. (2004). Gobiidae II. In P. J. Miller & P. S. Economidis (Eds.), The Freshwater Fishes of Europe (pp. 157–398). Aula-Verlag.
Mrakovčić, M., Brigić, A., Buj, I., Ćaleta, M., Mustafić, P., & Zanella, D. (2006). Red Book of Freshwater Fishes of Croatia. Ministarstvo kulture, Državni zavod za zaštitu prirode, 253 pp. (in Croatian with English abstract).
Mrakovčić, M., Kerovec, M., Mišetić, S., & Schneider, D. (1996). Description of Knipowitschia punctatissima croatica (Pisces: Gobiidae), a new freshwater goby from Dalmatia, Croatia. In A. Kirchhofer & D. Hefti (Eds.), Conservation of endangered freshwater fish in Europe (pp. 311–319). Birkhäuser Verlag.
Myers, N., Mittermeier, R., Mittermeier, C., Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. https://doi.org/10.1038/35002501
Myrberg, A. A., Spanier, E., & Ha, S. J. (1978). Temporal patterning in acoustical communication. In Contrasts in behavior (pp. 137–179). Wiley.
Myrberg, A. A., Jr. (1981). Sound communication and interception in fishes. In W. N. Tavolga, A. N. Popper, & R. R. Fay (Eds.), Hearing and communication in fishes (pp. 395–424). Springer-Verlag.
Myrberg, A. A., Jr., & Lugli, M. (2006). Reproductive behaviour and acoustical interactions. In F. Ladich, S. P. Collin, P. Moller, & B. G. Kapoor (Eds.), Communication in fishes, vol. 1 (pp. 149–176). Science Publishers.
Nelson, J. S., Grande, T. C., & Wilson, M. V. H. (2016). Fishes of the world (5th ed.). John Wiley and Sons. https://doi.org/10.1002/9781119174844
Otovic, P., & Partan, S. (2009). Multimodal signaling in animals. In L. R. Squire (Ed.), Encyclopedia of neuroscience (pp. 1095–1105). Academic Press.
Parmentier, E., & Fine, M. L. (2016). Fish sound production: Insight. In R. Suthers, T. C. Fitch, A. N. Popper, & R. R. Fay (Eds.), Vertebrate sound production and acoustic communication (pp. 19–49). Springer.
Parmentier, E., Kéver, L., Boyle, K., Corbisier, Y., 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., Kéver, L., Casadevall, M., & Lecchini, D. (2010). 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., Lecchini, D., Frederich, B., Brié, C., & Mann, D. (2009). Sound production in four damselfish (Dascyllus) species: Phyletic relationships. Biological Journal of the Linnean Society, 97, 928–940.
Parmentier, E., Petrinisec, M., Fonseca, P. J., & Amorim, M. C. P. (2017). Sound-production mechanism in Pomatoschistus pictus. Journal of Experimental Biology, 220, 4374–4376.
Pedroso, S. S., Barber, I., Svensson, O., Fonseca, P. J., Amorim, M. C. P., & Almada, V. C. (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
Rice, A. N., & Bass, A. H. (2009). Novel vocal repertoire and paired swimbladders of the three-spined toadfish, Batrachomoeus trispinosus: Insights into the diversity of the Batrachoididae. Journal of Experimental Biology, 212, 1377–1391. https://doi.org/10.1242/jeb.028506
Rice, A. N., Farina, S. C., Makowski, A. J., Kaatz, I. M., Lobel, P. S., & Bemis, W. E. (2020). Evolution and ecology in widespread acoustic signaling behavior across fishes. bioRxiv https://doi.org/10.1101/2020.09.14.296335
Rice, A. N., Farina, S. C., Makowski, A. J., Kaatz, I. M., Lobel, P. S., & Bemis, W. E. (2022). Evolutionary patterns in sound production across fishes. Ichthyology & Herpetology, 110(1), 1–12. https://doi.org/10.1643/i2020172
Rowell, T., Nemeth, R., Schärer, M., & Appeldoorn, R. (2015). Fish sound production and acoustic telemetry reveal behaviors and spatial patterns associated with spawning aggregations of two Caribbean groupers. Marine Ecology Progress Series, 518, 239–254.
Šanda, R., & Kovačić, M. (2009). Freshwater gobies in the Adriatic drainage basin of the Western Balkans. Annales. Series Historia Naturalis, 19(1), 1–10.
Thacker, C. E. (2009). Phylogeny of Gobioidei and placement within Acantomorpha with a new classification and investigation of diversification and character evolution. Copeia, 2009, 93–104.
Thacker, C. E., Gkenas, C., Triantafyllidis, A., Malavasi, S., Leonardos, I., & Leonardos, I. (2019). Phylogeny, systematics and biogeography of the European sand gobies (Gobiiformes: Gobionellidae). Zoological Journal of the Linnean Society, 185(1), 212–225. https://doi.org/10.1093/zoolinnean/zly026
Torricelli, P., Lugli, M., & Pavan, G. (1990). Analysis of sounds produced by male Padogobius martensi (pisces, Gobiidae) and factors affecting their structural properties. Bioacoustics, 2, 261–275. https://doi.org/10.1080/09524622.1990.9753141
Tougard, C., Vukić, J., Ahnelt, H., Buj, I., Kovačić, M., Moro, G., Tutman, P., & Šanda, R. (2021). Quaternary climatic cycles promoted (re)colonization and diversification events in Adriatic sand gobies. Journal of Zoological Systematics and Evolutionary Research, 59(3), 777–788. https://doi.org/10.1111/jzs.12468
Tutman, P., Zanella, D., Horvatić, S., Hamzić, A., Adrović, A., Dulčić, J., & Glamuzina, B. (2020). Freshwater gobies (Gobiidae) of Bosnia and Herzegovina: A review of the current status and distribution. Journal of Vertebrate Biology, 69(4), 1–15. https://doi.org/10.25225/jvb.20046
Vanhove, M., Kovačić, M., & Zogaris, S. (2016). A distinct Island population of threatened freshwater fish: To split or lump? Hydrobiologia, 777(1), 79–93. https://doi.org/10.1007/s10750-016-2765-z
Vanhove, M. P. M., Economou, A. N., Zogaris, S., Larmuseau, M. H. D., Giakoumi, S., Kalogianni, E., Volckaert, F. A. M., & Huyse, T. (2012). Phylogenetics and biogeography of the Balkan sand gobies' (Teleostei: Gobiidae): Vulnerable species in need of taxonomic revision. Biological Journal of the Linnean Society, 105, 73–91. https://doi.org/10.1111/j.1095-8312.2011.01781.x
Vicente, J. R., Fonseca, P. J., & Amorim, M. C. P. (2015). Effects of temperature on sound production in the painted goby Pomatoschistus pictus. Journal of Experimental Marine Biology and Ecology, 473, 1–6.
Winterbottom, R. (1974). A descriptive synonymy of the striated muscles of the Teleostei. Proceedings of the Academy of Natural Sciences of Philadelphia, 125, 225–317.
Zanella, D., Marčić, Z., Ćaleta, M., Buj, I., Zrnčić, S., Horvatić, S., & Mustafić, P. (2017). Early development of the freshwater goby Orsinogobius croaticus endemic to Croatia and Bosnia-Herzegovina. Cybium, 41(4), 335–342.
Zanella, D., Mrakovčić, M., Zanella, L. N., Miletić, M., Mustafić, P., Ćaleta, M., & Marčić, Z. (2011). Reproductive biology of the freshwater goby Knipowitschia croatica Mrakovčić, Kerovec, Mišetić & Schneider 1996 (Actinopterygii, Gobiidae). Journal of Applied Ichthyology, 27, 1242–1248.
Zanette, I., Daghfous, G., Weitkamp, T., Gillet, B., Adriaens, D., & Langer, M. (2013). Looking inside marine organisms with magnetic resonance and X-ray imaging. In E. G. Reynaud (Ed.), Imaging marine life (pp. 122–184). Wiley. https://doi.org/10.1002/9783527675418.ch7
Zeyl, J. N., Malavasi, S., Holt, D. E., Noel, P., Lugli, M., & Johnston, C. E. (2016). Convergent aspects of acoustic communication in darters, sculpins and gobies. In A. J. Sisneros (Ed.), Fish hearing and bioacoustics: An anthology in honor of Arthur N. Popper and Richard R. Fay (pp. 93–120). Springer.
