Skip to main content

Advertisement

Log in

Melatonin reduces aggressiveness and improves oxidative status of matrinxã (Brycon amazonicus) subjected to social challenge

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Melatonin is a hormone that can modulate aggressive interactions in fish, stimulate antioxidant enzymes, and neutralize the biological damage caused by high free radical production. Fish, especially those kept in artificial environments, are subject to damage caused by free radicals resulting from stressful conditions, such as a social challenge. The matrinxã (Brycon amazonicus) arouses great commercial interest and has been widely used in farming systems. However, these animals have a high frequency of aggressive behavior and cannibalism, which is considered a limiting factor for the production system. Thus, we evaluated the influence of melatonin on aggressiveness and oxidative stress parameters in matrinxã juveniles, testing whether melatonin increases glutathione concentrations and reduces lipid peroxidation (thiobarbituric acid–reactive substances) during social challenge. For this, 24 fish were subjected to three concentrations of melatonin in water: control (0 μmol/L), low MEL (1 μmol/L), and high MEL (10 μmol/L), with eight replicates each. The fish were isolated for 96 h, subjected to the mirror test (social challenge), and then euthanized and dissected to remove the liver. Melatonin reduced total aggressive interactions in animals treated with melatonin (P = 0.036), increased glutathione concentrations (P = 0.002), and decreased levels of lipid peroxidation (P = 0.001). We concluded that melatonin reduces aggressiveness and acts as a potent antioxidant in matrinxã juveniles, contributing to the reduction in stress levels and thus improving the maintenance conditions of animals in production systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allegra M, Reiter RJ, Tan DX, Gentile C, Tesoriere L, Livrea MA (2003) The chemistry of melatonin’s interaction with reactive species. J Pineal Res 34:1–10

    CAS  PubMed  Google Scholar 

  • Alvarenga CMD, Volpato GL (1995) Agonistic profile and metabolism in alevines of Nile tilapia. Physiol Behav 57:75–80

    CAS  PubMed  Google Scholar 

  • Beutler E (1984) Red cell metabolism: a manual of biochemical methods, 3rd edn. Grune & Straton, NY

    Google Scholar 

  • Biller-Takahashi JD, and Takahashi LS. (2016). Estresse oxidativo e sistema imune de peixes. In: Camargo ACS, Nogueira WCL, Torres AFB, Almeida AC, Stefanello CM (eds) Piscicultura - aspectos relevantes. Fundação Universidade Federal do Pampa, Rio Grande do Sul, pp 317-341

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Conde-Sieira M, Muñoz JLP, López-Patiño MA, Gesto M, Soengas JL, Míguez JM (2014) Oral administration of melatonin counteracts several of the effects of chronic stress in rainbow trout. Domest Anim Endocrinol 46:26–36

    CAS  PubMed  Google Scholar 

  • Conte FS (2004) Stress and the welfare of cultured fish. Appl Anim Behav Sci 86:205–223

    Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    CAS  PubMed  Google Scholar 

  • Di Giulio RT, Meyer JN (2008) Reactive oxygen species and oxidative stress. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press. Boca Raton, FL, pp 273-326

  • Falcón J, Besseau L, Magnanou E, Herrero MJ, Nagai M, Boeuf G (2011) Melatonin, the time keeper: biosynthesis and effects in fish. Cybium: International Journal of Ichthyology 35:3–18

    Google Scholar 

  • Ferraz FB, Gomes LC (2009) Social relationship as inducer of immunological and stress responses in matrinxã (Brycon amazonicus). Comp Biochem Physiol 153:293–296

    Google Scholar 

  • García JJ, Reiter RJ, Guerrero JM, Escames G, Yu BP, Oh CS, Muñoz-Hoyos A (1997) Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett 408:297–300

    PubMed  Google Scholar 

  • García JJ, Pingarrón LL, Souza PA, Tres A, Escudero P, García-Gil FA, Tan DX, Reiter RJ, Ramírez JM, Bernal-Pérez M (2014) Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J Pineal Res 56:225–237

    PubMed  Google Scholar 

  • Gonçalves-de-Freitas E, Mariguela TC (2006) Social isolation and aggressiveness in the amazonian juvenile fish Astronotus ocellatus. Braz J Biol 66:233–238

    PubMed  Google Scholar 

  • Gülçin I, Beydemir Ş, Hisar O, Köksal E, Reiter RJ (2009) Melatonin administration increases antioxidant enzymes activities and reduces lipid peroxidation in the rainbow trout (Oncorhynchus mykiss, Walbaum) erythrocytes. Turk J Vet Anim Sci 33:241–245

    Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. In: Halliwell B, Gutteridge JMC (eds) Free radicals in biology and medicine. Oxford University Press, Oxford, pp 1–25

    Google Scholar 

  • Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM, Pandi-Perumal SR (2011) Melatonin-a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 93:350–384

    CAS  PubMed  Google Scholar 

  • Hoglund E, Bakke MJ, Øverli Ø, Winberg S, Nilsson GE (2005) Suppression of aggressive behaviour in juvenile Atlantic cod, Gadus morhua by L-tryptophan supplementation. Aquaculture 249:525–531

    Google Scholar 

  • Inoue LAKA, Neto CS, Moraes G (2003) Clove oil as anaesthetic for juveniles of ‘matrinxã’ Brycon cephalus (Gunther, 1869). A ciência Rural 33:943–947

    Google Scholar 

  • Lepage O, Larson ET, Mayer I, Winberg S (2005) Serotonin, but not melatonin, plays a role in shaping dominant–subordinate relationships and aggression in rainbow trout. Horm Behav 48:233–242

    CAS  PubMed  Google Scholar 

  • López-Patiño MA, Conde-Sieira M, Gesto M, Librán-Pérez M, Soengas JL, Míguez JM (2013) Melatonin partially minimizes the adverse stress effects in senegalese sole (Solea senegalensis). Aquaculture 388-391:65–172

    Google Scholar 

  • Nimse SB, Pal D (2015) Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv 5:27986–28006

    CAS  Google Scholar 

  • Nordberg J, Arnér ESJ (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312

    CAS  PubMed  Google Scholar 

  • Oliveira RF, Gonçalves DM (2008) Hormones and social behaviour of teleost fish. In: Magnhagen C, Braithwaite VA, Forsgren E, Kapoor BG (eds) Fish behaviour. CRC Press. Boca Raton, FL, pp 61–125

    Google Scholar 

  • Oliveira RF, Carneiro LA, Canário AVM (2005) No hormonal response in tied fights. Nature 437:207–208

    CAS  PubMed  Google Scholar 

  • Pompella A (1997) Biochemistry and histochemistry of oxidant stress and lipid peroxidation. Int J Vitam Nutr Res 67:289–297

    CAS  PubMed  Google Scholar 

  • Popek W, Luszczek-Trojnar E, Dryg-Kozak E, Rzasa J, Epler P (2006) Effect of melatonin on dopamine secretion in the hypothalamus of mature female common carp, Cyprinus carpio L. Acta Ichthyol Piscat 36:135–141

    Google Scholar 

  • Ramis MR, Esteban S, Miralles A, Tan DX, Reiter RJ (2015) Protective effects of melatonin and mitochondria-targeted antioxidants against oxidative stress: a review. Curr Med Chem 22:2690–2711

    CAS  PubMed  Google Scholar 

  • Reiter RJ, Tan DX, Terron MP, Flores LJ, Czarnocki Z (2007) Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol 54:1–9

    CAS  PubMed  Google Scholar 

  • Reiter RJ, Tan DX, Rosales-Corral S, Galano A, Zhou XJ, Xu B (2018) Mitochondria: central organelles for melatonin’s antioxidant and anti-aging actions. Molecules 23:509

    PubMed Central  Google Scholar 

  • Sébert ME, Legros C, Weltzien FA, Malpaux B, Chemineau P, Dufour S (2008) Melatonin activates brain dopaminergic systems in the eel with an inhibitory impact on reproductive function. J Neuroendocrinol 20:917–929

    Google Scholar 

  • Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Eng 25:1058–1071

    Google Scholar 

  • Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    CAS  PubMed  Google Scholar 

  • Spix JBV, Agassiz L (1829) Selecta genera et species piscium quos in itinere per Brasiliam annos 1817-1820 jussu et auspiciis Maximiliani Josephi I. Selecta genera et species piscium brasiliensium

  • Storey KB (1996) Oxidative stress: animal adaptation in nature. Braz J Med Biol Res 29:1715–1733

    CAS  PubMed  Google Scholar 

  • Thomás-Zapico C, Coto-Montes A (2005) A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 39:99–104

    Google Scholar 

  • Urata Y, Honma S, Goto S, Todoroki S, Iida T, Cho S, Honma K, Kondo T (1999) Melatonin induces ʏ-glutamylcysteine synthetase mediated by activator protein-1 in human vascular endothelial cells. Free Radic Biol Med 27:838–847

    CAS  PubMed  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–189

    CAS  PubMed  Google Scholar 

  • Volpato GL, Barreto RE (2001) Environmental blue light prevents stress in the fish Nile tilapia. Braz J Med Biol Res 34:1041–1045

    CAS  PubMed  Google Scholar 

  • Wendelaar-Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

  • Winiarska K, Fraczyk T, Malinska D, Drozak J, Bryla J (2006) Melatonin mitigates diabetes-induced oxidative stress in rabbits. J Pineal Res 40:168–176

    CAS  PubMed  Google Scholar 

  • Wolkers CPB, Serra M, Hoshiba MA, Urbinati EC (2012) Dietary L-tryptophan alters aggression in juvenile matrinxã Brycon amazonicus. Fish Physiol Biochem 38:819–827

    CAS  PubMed  Google Scholar 

  • Zaniboni-Filho E, Tataje DR, Weingartner M (2006) Potencialidad del género Brycon em la piscicultura brasileña. Rev Colomb Cienc Pec 19:233–240

    Google Scholar 

  • Zar J (1999) Biostatistical analyses. Printice Hall, NJ

    Google Scholar 

Download references

Acknowledgments

The authors thank Damy Caroline de Melo Souza and Ândrocles Oliveira Borges for helping conduct the experiments and Msc. Yugo Moraes Pastrana for collaborating in the statistical analyses of the data.

Funding

The authors also thank the Amazonas Research Foundation (Fundação de Amparo à Pesquisa do Estado do Amazonas - FAPEAM) for financial support, process no. 015/2014-PAPAC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thaís Billalba Carvalho.

Ethics declarations

This study was conducted in accordance with the Ethical Principles on Animal Experimentation adopted by the National Council of Animal Experimentation (Conselho Nacional de Experimentação Animal - CONCEA) and approved by the Ethics Committee on Animal Use of the Federal University of Amazonas (UFAM), Manaus, AM, Brazil, protocol no. 019/2015.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Amaral, A.P., da Silva, E.C.C. & Carvalho, T.B. Melatonin reduces aggressiveness and improves oxidative status of matrinxã (Brycon amazonicus) subjected to social challenge. Fish Physiol Biochem 46, 1019–1024 (2020). https://doi.org/10.1007/s10695-020-00768-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00768-x

Keywords

Navigation