Muscular hypertrophy of urinary bladders in dominant tilapia facilitates the control of aggression through urinary signals

In: Behaviour

The urination pattern of the Mozambique tilapia (Oreochromis mossambicus) depends on social context, and the olfactory potency of urine released depends on social rank (males) and reproductive status (females). This strongly suggests that urine mediates chemical communication in this species. The current study tested, firstly, whether urine production rate depends on sex or social status and, secondly, whether differences in urination pattern and volume of urine stored are associated with variation in the morphology of the urinary bladder. Finally, the effect of urination during aggressive male–male interactions was assessed. Urine production in catheterized fish depended neither on sex nor social status (males). Nevertheless, males had larger kidneys than females. Dominant males had heavier urinary bladders than subordinate males or females, mainly due to enlarged muscle fibres, thicker urothelium and a thicker smooth muscle layer. In male pairs wherein urination was prevented by temporary constriction of the genital papillae, social interaction escalated to aggression (mouth-to-mouth fighting) more rapidly and frequently than control pairs. This was accompanied by elevated plasma testosterone and 11-ketotestosterone levels. In control encounters, the male that initiated the aggressive behaviour was usually the winner of the subsequent fight; this did not happen when the males could not urinate. These results suggest that the larger, more muscular bladder of dominant males is an adaptation, facilitating higher urination frequency, post-renal modulation and storage of larger urine volumes for longer. It is likely that urinary pheromones modulate aggression in male–male encounters by providing information on the social rank and/or motivation of the emitter; males are unlikely to invest in costly highly aggressive fights if they judge their opponent to be more dominant. Thus, a morphological explanation for the differing urination patterns of dominant and subordinant males, and females, has been provided, and a possible function for this behaviour in male–male interactions is suggested.

  • AlmeidaO.G.MirandaA.HubbardP.C.FradeP.BarataE.N.CanárioA.V.M. (2005). Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). — Chem. Senses 30: i309-i310.

    • Search Google Scholar
    • Export Citation
  • AmorimM.C.P.FonsecaP.J.AlmadaV.C. (2003). Sound production during courtship and spawning of Oreochromis mossambicus: male–female and male–male interactions. — J. Fish Biol. 62: 658-672.

    • Search Google Scholar
    • Export Citation
  • AppeltC.W.SorensenP.W. (2007). Female goldfish signal spawning readiness by altering when and where they release a urinary pheromone. — Anim. Behav. 74: 1329-1338.

    • Search Google Scholar
    • Export Citation
  • BarataE.N.FineJ.M.HubbardP.C.AlmeidaO.G.FradeP.SorensenP.W.CanárioA.V.M. (2008). A sterol-like odorant in the urine of Mozambique tilapia males likely signals social dominance to females. — J. Chem. Ecol. 34: 438-449.

    • Search Google Scholar
    • Export Citation
  • BarataE.N.HubbardP.C.AlmeidaO.G.MirandaA.CanárioA.V.M. (2007). Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus, Peters 1852). — BMC Biology 5: 54.

    • Search Google Scholar
    • Export Citation
  • BreithauptT. (2011). Chemical communication in crayfish. — In: Chemical communication in crustaceans ( BreithauptT.ThielM. eds). SpringerNew York, NY p.  257-276.

    • Search Google Scholar
    • Export Citation
  • BreithauptT.EgerP. (2002). Urine makes the difference: chemical communication in fighting crayfish made visible. — J. Exp. Biol. 205: 1221-1231.

    • Search Google Scholar
    • Export Citation
  • BreithauptT.LindstromD.P.AtemaJ. (1999). Urine release in freely moving catheterised lobsters (Homarus americanus) with reference to feeding and social activities. — J. Exp. Biol. 202: 837-844.

    • Search Google Scholar
    • Export Citation
  • BrennanP.A.ZufallF. (2006). Pheromonal communication in vertebrates. — Nature 444: 308-315.

  • BrutonM.N.BolttR.E. (1975). Aspects of the biology of Tilapia mossambica Peters (Pisces: Cichlidae) in a natural freshwater lake (Lake Sibaya, South Africa). — J. Fish Biol. 7: 423-445.

    • Search Google Scholar
    • Export Citation
  • CardwellJ.R.LileyN.R. (1991). Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae). — Horm. Behav. 25: 1-18.

    • Search Google Scholar
    • Export Citation
  • ChenX.G.BrodlandG.W. (2009). Mechanical determinants of epithelium thickness in early-stage embryos. — J. Mech. Behav. Biomed. Mater. 2: 494-501.

    • Search Google Scholar
    • Export Citation
  • CondeçaJ.B.CanarioA.V.M. (1999). The effect of estrogen on the gonads and on in vitro conversion of androstenedione to testosterone, 11-ketotestosterone, and estradiol-17β in Sparus aurata (Teleostei, Sparidae). — Gen. Comp. Endocrinol. 116: 59-72.

    • Search Google Scholar
    • Export Citation
  • DrickamerL.C. (1995). Rates of urine excretion by house mouse (Mus domesticus) — differences by age, sex, social-status, and reproductive condition. — J. Chem. Ecol. 21: 1481-1493.

    • Search Google Scholar
    • Export Citation
  • Gonçalves-de-FreitasE.TeresaF.B.GomesF.S.GiaquintoP.C. (2008). Effect of water renewal on dominance hierarchy of juvenile Nile tilapia. — Appl. Anim. Behav. Sci. 112: 187-195.

    • Search Google Scholar
    • Export Citation
  • GotoA.HasegawaT.YamazakiF. (1979). Secretory granules in the renal tubules of male fresh-water sculpin, Cottus hangiongensis, during the spawning period. — Jpn. J. Ichthyol. 26: 302-307.

    • Search Google Scholar
    • Export Citation
  • HirschenhauserK.TaborskyM.OliveiraT.CanárioA.V.M.OliveiraR.F. (2004). A test of the ‘challenge hypothesis’ in cichlid fish: simulated partner and territory intruder experiments. — Anim. Behav. 68: 741-750.

    • Search Google Scholar
    • Export Citation
  • HumphriesR.E.RobertsonD.H.L.BeynonR.J.HurstJ.L. (1999). Unravelling the chemical basis of competitive scent marking in house mice. — Anim. Behav. 58: 1177-1190.

    • Search Google Scholar
    • Export Citation
  • HurstJ.L.BeynonR.J. (2004). Scent wars: the chemobiology of competitive signalling in mice. — Bioassays 26: 1288-1298.

  • IkedaK. (1933). Effect of castration on the secundary sexual characters of anadromous three-spined stickleback Gasterosteus aculeatus (L.). — Jpn. J. Zool. 5: 135-157.

    • Search Google Scholar
    • Export Citation
  • KimeD.E.ManningN.J. (1982). Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. — Gen. Comp. Endocrinol. 48: 222-231.

    • Search Google Scholar
    • Export Citation
  • MaruskaK.P.FernaldR.D. (2012). Contextual chemosensory urine signaling in an African cichlid fish. — J. Exp. Biol. 215: 68-74.

  • MirandaA.AlmeidaO.G.HubbardP.C.BarataE.N.CanárioA.V.M. (2005). Olfactory discrimination of female reproductive status by male tilapia (Oreochromis mossambicus). — J. Exp. Biol. 208: 2037-2043.

    • Search Google Scholar
    • Export Citation
  • Mucignat-CarettaC.BondiM.CarettaA. (2004). Endocrine status affects bladder size and postvoid residual urinary volume in mice. — Horm. Behav. 46: 11-18.

    • Search Google Scholar
    • Export Citation
  • OliveiraR.F.AlmadaV.C. (1996). On the (in)stability of dominance hierarchies in the cichlid fish Oreochromis mossambicus. — Aggr. Behav. 22: 37-45.

    • Search Google Scholar
    • Export Citation
  • OliveiraR.F.AlmadaV.C. (1999). Male display characters, gonadal maturation and androgens in the cichlid fish Oreochromis mossambicus. — Acta Ethol. 2: 67-70.

    • Search Google Scholar
    • Export Citation
  • OliveiraR.F.AlmadaV.C.CanarioA.V.M. (1996). Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus. — Horm. Behav. 30: 2-12.

    • Search Google Scholar
    • Export Citation
  • OliveiraR.F.CarneiroL.A.CanárioA.V.M. (2005). No hormonal response in tight fights. — Nature 437: 207-208.

  • RosA.F.H.BeckerK.OliveiraR.F. (2006). Aggressive behaviour and energy metabolism in a cichlid fish, Oreochromis mossambicus. — Physiol. Behav. 89: 164-170.

    • Search Google Scholar
    • Export Citation
  • SchneiderR.A.Z.HuberR.MooreP.A. (2001). Individual and status recognition in the crayfish, Orconectes rusticus: the effects of urine release on fight dynamics. — Behaviour 138: 137-153.

    • Search Google Scholar
    • Export Citation
  • ScottA.P.MackenzieD.S.StaceyN.E. (1984). Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. 2. Steroid hormones. — Gen. Comp. Endocrinol. 56: 349-359.

    • Search Google Scholar
    • Export Citation
  • SlomanK.A.ScottG.R.McDonaldD.G.WoodC.M. (2004). Diminished social status affects ionoregulation at the gills and kidney in rainbow trout (Oncorhynchus mykiss). — Can. J. Fish. Aquat. Sci. 61: 618-626.

    • Search Google Scholar
    • Export Citation
  • StaceyN.SorensenP. (2002). Hormonal pheromones in fish. — In: Hormones brain and behavior ( PfaffD.W.ArnoldA.P.EtgenA.M.FahrbachS.E.RubinR.T. eds). Academic PressNew York, NY p.  375-434.

    • Search Google Scholar
    • Export Citation
  • SummerfeltR.C.SmithL.S. (1990). Anesthesia, surgery, and related techniques. — In: Methods for fish biology ( SchreckC.B.MoyleP.B. eds). American Fisheries SocietyBethesda, MD p.  213-272.

    • Search Google Scholar
    • Export Citation
  • TurnerG.F. (1986). Territory dynamics and cost of reproduction in a captive population of the colonial nesting mouthbrooder Oreochromis mossambicus (Peters). — J. Fish Biol. 29: 573-587.

    • Search Google Scholar
    • Export Citation
  • WardA.J.W.MehnerT. (2010). Multimodal mixed messages: the use of multiple cues allows greater acuaracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. — Behav. Ecol. 21: 1315-1320.

    • Search Google Scholar
    • Export Citation
  • WoodC.M.PatrickM.L. (1994). Methods for assessing kidney and urinary bladder function in fish. — In: Biochemistry and molecular biology of fishes: analytical techniques ( HochachkaP.W.MommsenT.P. eds). ElsevierLondon p.  127-143.

    • Search Google Scholar
    • Export Citation
  • YamazakiF.WatanabeK. (1979). The role of steroid hormones in sex recognition during spawning behaviour of the goldfish, Carassius auraius L.Proc. Indian Nat. Sci. Acad. 45: 505-511.

    • Search Google Scholar
    • Export Citation
  • YambeH.YamazakiF. (2006). Transitions of urine flow rate and kidney-somatic index in mature masu salmon. — Fish. Sci. 72: 1048-1053.

    • Search Google Scholar
    • Export Citation

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