Acoustic signals produced by Nile tilapia Oreochromis niloticus and black-chinned tilapia Sarotherodon melanotheron during intra- and interspecific pairings
[en] We characterised, for the first-time, the sound production of black-chinned tilapia Sarotherodon melanotheron and show differences with that of Nile tilapia Oreochromis niloticus in a hybridization pairing context. Although both species were able to produce drum sounds, they showed different acoustic features. Drum sounds were produced in aggressive (chasing or lateral attack) and non-aggressive (courtship) contexts by O. niloticus but only in aggressive situations (fleeing or avoidance) by S. melanotheron. The second type of sounds produced by O. niloticus were grunts, produced in both aggressive (chasing and after biting) and non-aggressive contexts (nest building). The second type of sound produced by S. melanotheron was a rolling sound, produced only during courtship. Each species was able to produce common sounds (drum) and species-specific sounds (grunts and rolling). This implies that species can communicate without being able to understand each other because the sounds emitted may probably have different significance. Drumming corresponded only to aggressivity in S. melanotheron, whereas this was not true for O. niloticus. 11-ketotestosterone (11-kt) levels were significantly higher in male O. niloticus than male S. melanotheron, but there was no significant correlation between 11-kt or estradiol concentrations and the number of sounds produced in aggressive or non-aggressive behavioural contexts in either species. During interspecies interactions, O. niloticus drum sounds are likely considered to be aggressive by S. melanotheron and could potentially constitute a reproductive barrier between the two species.
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 :
Akian, D
Yao, K
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Joassard, L
Clota, F
Baroillier, JF
Lozano, P
Chatain, B
Bégout, ML
Language :
English
Title :
Acoustic signals produced by Nile tilapia Oreochromis niloticus and black-chinned tilapia Sarotherodon melanotheron during intra- and interspecific pairings
Adepo-Gourene, B., Gourene, G., Différenciation morphologique des populations naturelles d'une sous-espèce de tilapia Sarotherodon melanotheron melanotheron Rüppell, 1852 (Teleostei; Cichlidae) de Côte d'Ivoire. Sciences et Nature 5 (2008), 15–27.
Akian, D.D., Yao, K., Clota, F., Lozano, P., Baroiller, J.F., Chatain, B., Bégout, M.-L., Reproductive behaviour of two tilapia species (Oreochromis niloticus, Linné, 1758; Sarotherodon melanotheron, Rüppel, 1852) in freshwater intra and interspecific pairing context. Appl. Anim. Behav. Sci. 193 (2017), 104–113.
Amorim, M.C.P., Diversity of sound production in fish. Communication in Fishes 1 (2006), 71–104.
Amorim, M.C.P., Almada, V.C., The outcome of male–male encounters affects subsequent sound production during courtship in the cichlid fish Oreochromis mossambicus. Anim. Behav. 69 (2005), 595–601.
Amorim, M.C.P., Neves, A.S.M., Acoustic signalling during courtship in the painted goby, Pomatoschistus pictus. J. Mar. Biol. Assoc. UK 87 (2007), 1017–1023.
Amorim, M.C.P., Neves, A.S.M., Male painted gobies (Pomatoschistus pictus) vocalise to defend territories. Behaviour 145 (2008), 1065–1083.
Amorim, M.C.P., Fonseca, P.J., Almada, V.C., Sound production during courtship and spawning of Oreochromis mossambicus: male–female and male–male interactions. J. Fish Biol. 62 (2003), 658–672.
Amorim, M.C.P., Knight, M.E., Stratoudakis, Y., Turner, G.F., Differences in sounds made by courting males of three closely related Lake Malawi cichlid species. J. Fish Biol. 65 (2004), 1358–1371.
Amorim, M.C.P., Simões, J.M., Fonseca, P.J., Turner, G.F., Species differences in courtship acoustic signals among five Lake Malawi cichlid species (Pseudotropheus spp.). J. Fish Biol. 72 (2008), 1355–1368.
Balshine-Earn, S., Reproductive rates, operational sex ratios and mate choice in St. Peter's fish. Behav. Ecol. Sociobiol. 39 (1996), 107–116.
Bégout, M.-L., Kadri, S., Huntingford, F., Damsgård, B., Tools for studying the behaviour of farmed fish. Aquacult. Behav, 2012, 65–86.
Bentley, G.E., Jensen, J.P., Kaur, G.J., Wacker, D.W., Tsutsui, K., Wingfield, J.C., Rapid inhibition of female sexual behavior by gonadotropin-inhibitory hormone (GnIH). Horm. Behav. 49 (2006), 550–555.
Bertucci, F., Beauchaud, M., Attia, J., Mathevon, N., Sounds modulate males’ aggressiveness in a cichlid fish. Ethology 116 (2010), 1179–1188.
Biswas, A.K., Morita, T., Yoshizaki, G., Maita, M., Takeuchi, T., Control of reproduction in Nile tilapia Oreochromis niloticus (L.) by photoperiod manipulation. Aquaculture 243 (2005), 229–239.
Candolin, U., The use of multiple cues in mate choice. Biol. Rev 78 (2003), 575–595.
Castro, A.L.S., Gonçalves-de-Freitas, E., Volpato, G.L., Oliveira, C., Visual communication stimulates reproduction in Nile tilapia, Oreochromis niloticus (L.). Braz. J. Med. and Biol. Res. 42 (2009), 368–374.
Consten, D., Lambert, J.G.D., Goos, H.T., Cortisol affects testicular development in male common carp, Cyprinus carpio L., but not via an effect on LH Secretion. Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. 129 (2001), 671–677.
Dunz, A.R., Schliewen, U.K., Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Mol. Phylogenetics Evol. 68 (2013), 64–80.
Johnson, N.S., Li, W., Understanding behavioral responses of fish to pheromones in natural freshwater environments. J. Comp. Physiol 196 (2010), 701–711.
Kishida, M., Specker, J.L., Paternal mouthbrooding in the black-chinned tilapia, Sarotherodon melanotheron (Pisces: Cichlidae): changes in gonadal steroids and potential for vitellogenin transfer to larvae. Horm. Behav. 37 (2000), 40–48.
Kobayashi, M., Aida, K., Hanyu, I., Hormone changes during ovulation and effects of steroid hormones on plasma gonadotropin levels and ovulation in goldfish. Gen. Comp. Endocr. 67 (1987), 24–32.
Koné, T., Teugels, G.G., N'Douba, V., Gooré, B.G., Kouamélan, E.P., Premières données sur l'inventaire et la distribution de l'ichtyofaune d'un petit bassin côtier Ouest Africain : Rivière Gô (Côte d'Ivoire). Cybium 27 (2003), 101–106.
Legendre, M., Trébaol, L., Efficacité de l'incubation buccale et fréquence de ponte de Sarotherodon melanotheron (Rüppel, 1852) en milieu d’élevage (lagune Ebrié, Côte d'Ivoire). Pullin, R.S.V., Lazard, J., Legendre, M., Amon Kothias, J.B., Pauly, et D., (eds.) Le Troisième Symposium International sur le Tilapia en Aquaculture. ICLARM Conf. Proc., 41, 1996, ICLARM Conf. Proc, 375–386.
Lobel, P.S., Possible species specific courtship sounds by two sympatric cichlid fishes in Lake Malawi. Africa. Environ. Biol. Fishes 52 (1998), 443–452.
Longrie, N., Fine, M.L., Parmentier, E., Innate sound production in the cichlid Oreochromis niloticus. J. Zool. 275 (2008), 413–417.
Longrie, N., Van Wassenbergh, S., Vandewalle, P., Mauguit, Q., Parmentier, E., Potential mechanism of sound production in Oreochromis niloticus (Cichlidae). J. Exp. Biol. 212 (2009), 3395–3402.
Longrie, N., Poncin, P., Denoël, M., Gennotte, V., Delcourt, J., Parmentier, E., Behaviours associated with acoustic communication in Nile Tilapia (Oreochromis niloticus). PLoS ONE, 8, 2013, e61467.
Machnik, P., Kramer, B., Female choice by electric pulse duration: attractiveness of the males’ communication signal assessed by female bulldog fish, Marcusenius pongolensis (Mormyridae, Teleostei). J. Exp. Biol. 211 (2008), 1969–1977.
Maruska, K.P., Ung, U.S., Fernald, R.D., The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance. PLoS ONE, 7, 2012, e37612.
Moyle, P.B., Cech, J.J. Jr, Fishes: An Introduction to Ichthyology. fourth ed., 2000, Prentice Hall, Upper Saddle River, NJ.
Munakata, A., Kobayashi, M., Endocrine control of sexual behavior in teleost fish. Gen. Comp. Endocr. 165 (2010), 456–468.
Munakata, A., Amano, M., Ikuta, K., Kitamura, S., Aida, K., The involvement of sex steroid hormones in downstream and upstream migratory behavior of Masu salmon. Comp. Biochem. Physiol. B 129 (2001), 661–669.
Nagl, S., Tichy, H., Mayer, W.E., Samonte, I.E., McAndrew, B.J., Klein, J., Classification and phylogenetic relationships of African tilapiine fishes inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 20:3 (2001), 361–374.
Oliveira, R.F., Social modulation of androgens in vertebrates: mechanisms and function. Slater, P.J.B., Rosenblatt, J.S., Snowdon, C.T., Roper, T.J., (eds.) Advances in the Study of Behavior, 34, 2004, Academic Press, New York, 165–239.
Onumah, E.E., Wessels, S., Wildenhayn, N., Brümmer, B., Schwark, H.G., Stocking density and photoperiod manipulation in relation to Estradiol profile to enhance spawning activity in female Nile Tilapia. Turk. J. Fish Aquat. Sc. 10 (2010), 463–470.
Parikh, V., Clement, T., Fernald, R., Androgen level and male social status in the African cichlid, Astatotilapia burtoni. Behav. Brain Res. 166 (2006), 291–295.
Parmentier, E., Fine, M., Vandewalle, P., Ducamp, J.-J., Lagardère, J.-P., Sound production in two carapids (Carapus acus and C. mourlani) and through the sea cucumber tegument. Acta Zool. 87 (2006), 113–119.
Patek, S.N., Shipp, L.E., Staaterman, E.R., The acoustics and acoustic behavior of the California spiny lobster (Panulirus interruptus). J. Acoust. Soc. Am. 125 (2009), 3434–3443.
Pedroso, S.S., Barber, I., Svensson, O., Fonseca, P.J., Amorim, M.C.P., Courtship sounds advertise species identity and male quality in sympatric Pomatoschistus spp. Gobies. PLoS ONE, 8, 2013, e64620.
Plenderleith, M., Oosterhout, Cv., Robinson, R.L., Turner, G.F., Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish. Biol. Lett. 1 (2005), 411–414.
Popper, A.N., Scanning electron microscopic study of sacculus and lagena in ears of fifteen species of teleost fishes. J. Morphol. 153 (1977), 397–417.
Ptacek, M.B., The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates. Behav. Process. 51:1-3 (2000), 111–134.
Remage-Healey, L., Rapid, hierarchical modulation of vocal patterning by steroid hormones. J. Neurosci. 24 (2004), 5892–5900.
Remage-Healey, L., Bass, A.H., Plasticity in brain sexuality is revealed by the rapid actions of steroid hormones. J. Neurosci. 27 (2007), 1114–1122.
Schulz-Mirbach, T., Heß, M., Metscher, B.D., Ladich, F., A unique swim bladder-inner ear connection in a teleost fish revealed by a combined high-resolution microtomographic and three-dimensional histological study. BMC Biol., 11, 2013, 75.
Smith, M.E., Kane, A.S., Popper, A.N., Acoustical stress and hearing sensitivity in fishes: does the linear threshold shift hypothesis hold water?. J. Exp. Biol. 207 (2004), 3591–3602.
Specker, J.L., Kishida, M., Mouthbrooding in the black-chinned tilapia, Sarotherodon melanotheron (Pisces: Cichlidae): The presence of eggs reduces androgen and estradiol levels during paternal and maternal parental behavior. Horm. Behav. 38 (2000), 44–51.
Tacon, P., Baroiller, J.F., Le Bail, P., Prunet, P., Jalabert, B., Effect of egg deprivation on sex steroids, gonadotropin, prolactin, and growth hormone profiles during the reproductive cycle of the mouthbrooding cichlid fish Oreochromis niloticus. Gen. Comp. Endocr. 117 (2000), 54–65.
Taves, M.D., Desjardins, J.K., Mishra, S., Balshine, S., Androgens and dominance: Sex-specific patterns in a highly social fish (Neolamprologus pulcher). Gen. Comp. Endocr. 161 (2009), 202–207.
Toguyeni, A., Fauconneau, B., Melard, C., Fostier, A., Lazard, J., Baras, E., Kuhn, E., van der Geyten, S., Baroiller, J.-F., Sexual dimorphism in two pure Cichlid species, Oreochromis niloticus niloticus (Linnaeus 1758) and Sarotherodon melanotheron melanotheron Ruppel 1852, and their intergeneric hybrids. Afr. J. Aquat. Sci. 34 (2009), 69–75.
Trewavas, E., Tilapine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia. 1983, Natural History, British Museum. London 583 p.
Tsutsui, K., Osugi, T., Evolutionary origin and divergence of GnIH and its homologous peptides. Gen. Comp. Endocr. 161 (2009), 30–33.
Vasconcelos, R.O., Carrico, R., Ramos, A., Modesto, T., Fonseca, P.J., Amorim, M.C.P., Vocal behavior predicts reproductive success in a teleost fish. Behav. Ecol. 23 (2012), 375–383.
Verzijden, M.N., van Heusden, J., Bouton, N., Witte, F., ten Cate, C., Slabbekoorn, H., Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences. Behav. Ecol. 21 (2010), 548–555.
Vignal, C., Kelley, D., Significance of temporal and spectral acoustic cues for sexual recognition in Xenopus laevis. Proc. R. Soc. B: Biol. Sci. 274 (2007), 479–488.
Yambe, H., Kitamura, S., Kamio, M., Yamada, M., Matsunaga, S., Fusetani, N., Yamazaki, F., L-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc. Natl. Acad. Sci. 103:3 (2006), 15370–15374.