Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 885–893 | Cite as

Meagre’s melatonin profiles under captivity: circadian rhythmicity and light sensitiveness

  • Catarina C. V. Oliveira
  • Filipe Figueiredo
  • Florbela Soares
  • Wilson Pinto
  • Maria Teresa Dinis
Article

Abstract

The present study reveals the first characterization of the plasma melatonin rhythms of the meagre (Argyrosomus regius) under aquaculture conditions. Melatonin levels were monitored during a 24 h cycle under a photoperiod of 16 L:8D and under constant darkness (DD), respectively to characterize the daily rhythm of this indoleamine and to test its endogenous origin. Besides, to identify which light intensities are perceived as night or day by this species, the degree of inhibition of nocturnal melatonin production caused by increasing intensities of light was tested (3.3, 5.3, 10.5, and 120 μW/cm2), applying 1 h light pulses at Mid-Dark. The result for melatonin daily rhythm in plasma showed a typical profile: concentration remained low during all daytime points, increasing greatly during dark points, with maximum values at 16:00 and 22:00 h, zeitgeber time. Under DD conditions, the plasma melatonin profile persisted, with a similar acrophase but with a lower amplitude between subjective day and night periods, indicating this rhythm as being endogenously driven. Moreover, meagre seemed to be very sensitive to dim levels of illumination during the night, since an intensity of just 3.3 μW/cm2 inhibited melatonin production. However, only the pulse of 5.3 μW/cm2 caused a melatonin drop till daytime concentrations. Thus, the threshold of light detection by the pineal organ was suggested as being located between 3.3 and 5.3 μW/cm2. Such results are an added value for this species biology knowledge, and in consequence to its adaptation to aquaculture conditions, allowing the improvement of culture husbandry protocols.

Keywords

Argyrosomus regius Pineal organ Daily rhythms Photoperiod Artificial lightning Melatonin inhibition 

Notes

Acknowledgements

This research has been financed by Projects AQUACOR (PROMAR 31-03-05FEP-003) and Prospawn (Seventh Framework Programme for Research and Technological Development, FP7/SME/2008/1), and CO is conceded an FCT grant (Fundação para a Ciência e Tecnologia, SFRH/BPD/63933/2009). Authors would also like to thank Marisa Barata for her help during fish maintenance.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Research involving animals

As stated in material and methods section, experiments were performed before the entry into force of Directive 2010/63/EU (EU 2010) as national legislation in Portugal. Nonetheless, no harmful procedures were applied to live animals and fish were reared according to the best practice. Whenever necessary, experimental procedures were performed under anesthesia and every effort was made to minimize suffering at all stages.

References

  1. Bayarri MJ, Madrid JA, Sánchez-Vázquez FJ (2002) Influence of light intensity, spectrum and orientation on sea bass plasma and ocular melatonin. J Pineal Res 32:34–40.  https://doi.org/10.1034/j.1600-079x.2002.10806.x CrossRefPubMedGoogle Scholar
  2. Bayarri MJ, García-Allegue R, López-Olmeda JF, Madrid JA, Sánchez-Vázquez FJ (2004) Circadian melatonin release in vitro by european sea bass pineal. Fish Physiol Biochem 30:87–89.  https://doi.org/10.1007/s10695-004-6002-8 CrossRefGoogle Scholar
  3. Bernier NJ, Van Der Kraak G, Farrell AP, Brauner CJ (2009) Fish neuroendocrinology. vol 28. Fish Physiology, 1st edn. Academic Press, LondonGoogle Scholar
  4. Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98.  https://doi.org/10.1016/S0044-8486(01)00583-X CrossRefGoogle Scholar
  5. Cermakian N, Sassone-Corsi P (2002) Environmental stimulus perception and control of circadian clocks. Curr Opin Neurobiol 12:359–365.  https://doi.org/10.1016/S0959-4388(02)00347-1 CrossRefPubMedGoogle Scholar
  6. Couto A, Barroso C, Guerreiro I, Pousão-Ferreira P, Matos E, Peres H, Oliva-Teles A, Enes P (2016) Carob seed germ meal in diets for meagre (Argyrosomus regius) juveniles: growth, digestive enzymes, intermediary metabolism, liver and gut histology. Aquaculture 451:396–404.  https://doi.org/10.1016/j.aquaculture.2015.10.007 CrossRefGoogle Scholar
  7. Díez A (2007) Representación grafica y análisis de datos en cronobiología. In: Madrid JA, Rol de Lama MA (eds) Cronobiología básica y clínica. Editec@red S.L., Madrid, pp 84–121Google Scholar
  8. Duncan N, Estévez A, Porta J, Carazo I, Norambuena F, Aguilera C, Gairin I, Bucci F, Valles R, Mylonas CC (2012) Reproductive development, GnRHa-induced spawning and egg quality of wild meagre (Argyrosomus regius) acclimatised to captivity. Fish Physiol Biochem 38:1273–1286.  https://doi.org/10.1007/s10695-012-9615-3 CrossRefPubMedGoogle Scholar
  9. Duncan NJ, Estévez A, Fernández-Palacios H, Gairin I, Hernández-Cruz CM, Roo J, Schuchardt D, Vallés R (2013) 17 - Aquaculture production of meagre (Argyrosomus regius): hatchery techniques, ongrowing and market. In: Allan G, Burnell G (eds) Advances in aquaculture hatchery technology. Woodhead Publishing, Sawston, Cambridge, UK, pp 519–541.  https://doi.org/10.1533/9780857097460.3.519
  10. Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer Associates Inc., MassachussettsGoogle Scholar
  11. Ekström P, Meissl H (1997) The pineal organ of teleost fish. Rev Fish Biol Fisher 7:199–284.  https://doi.org/10.1023/A:1018483627058 CrossRefGoogle Scholar
  12. EU (2010) Directive 2010/63/EU of the European Parliament and of the council of 22 September 2010 on the protection of animals used for scientific purposes, EN ed.; Union, E., Ed. Official Journal of European Union, Vol. L276, pp. 33–79Google Scholar
  13. Falcón J, Migaud H, Muñoz-Cueto JA, Carrillo M (2010) Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol 165:469–482.  https://doi.org/10.1016/j.ygcen.2009.04.026 CrossRefPubMedGoogle Scholar
  14. Fanouraki E, Mylonas CC, Papandroulakis N, Pavlidis M (2011) Species specificity in the magnitude and duration of the acute stress response in Mediterranean marine fish in culture. Gen Comp Endocrinol 173:313–322.  https://doi.org/10.1016/j.ygcen.2011.06.004 CrossRefPubMedGoogle Scholar
  15. Forsell J, Ekström P, Flamarique IN, Holmqvist BO (2001) Expression of pineal ultraviolet- and green-like opsins in the pineal organ and retina of teleosts. J Exp Biol 204:2517–2525PubMedGoogle Scholar
  16. García-Mesa S, Suárez MD, Rodríguez-Rúa A, Cárdenas S, García-Gallego M (2014) Productive and physiological implications of different feeding frequencies in meagre Argyrosomus regius (Asso, 1801). Aquac Eng 60:6–13.  https://doi.org/10.1016/j.aquaeng.2014.03.003 CrossRefGoogle Scholar
  17. Iigo M, Abe T, Kambayashi S, Oikawa K, Masuda T, Mizusawa K, Kitamura S, Azuma T, Takagi Y, Aida K, Yanagisawa T (2007) Lack of circadian regulation of in vitro melatonin release from the pineal organ of salmonid teleosts. Gen Comp Endocrinol 154:91–97.  https://doi.org/10.1016/j.ygcen.2007.06.013 CrossRefPubMedGoogle Scholar
  18. Martinez-Chavez CC, Al-Khamees S, Campos-Mendoza A, Penman DJ, Migaud H (2008) Clock-controlled endogenous melatonin rhythms in Nile tilapia (Oreochromis niloticus niloticus) and African catfish (Clarias gariepinus). Chronobiol Int 25:31–49.  https://doi.org/10.1080/07420520801917547 CrossRefPubMedGoogle Scholar
  19. Migaud H, Taylor JF, Taranger GL, Davie A, Cerd J, Carrillo M, Hansen T, Bromage N (2006) A comparative ex vivo and in vivo study of day and night perception in teleosts species using the melatonin rhythm. J Pineal Res 41:42–52.  https://doi.org/10.1111/j.1600-079X.2006.00330.x CrossRefPubMedGoogle Scholar
  20. Millán-Cubillo AF, Martos-Sitcha JA, Ruiz-Jarabo I, Cárdenas S, Mancera JM (2016) Low stocking density negatively affects growth, metabolism and stress pathways in juvenile specimens of meagre (Argyrosomus regius, Asso 1801). Aquaculture 451:87–92.  https://doi.org/10.1016/j.aquaculture.2015.08.034 CrossRefGoogle Scholar
  21. Molina-Borja M, Falcón J, Ravault JP (1996) Production of melatonin by the gilthead sea bream pineal: an in vivo and in vitro study. Fish Physiol Biochem 15:413–419.  https://doi.org/10.1007/bf01875584 CrossRefPubMedGoogle Scholar
  22. Mylonas CC, Salone S, Biglino T, de Mello PH, Fakriadis I, Sigelaki I, Duncan N (2016) Enhancement of oogenesis/spermatogenesis in meagre Argyrosomus regius using a combination of temperature control and GnRHa treatments. Aquaculture 464:323–330.  https://doi.org/10.1016/j.aquaculture.2016.07.006 CrossRefGoogle Scholar
  23. Nakahara D, Nakamura M, Iigo M, Okamura H (2003) Bimodal circadian secretion of melatonin from the pineal gland in a living CBA mouse. Proc Natl Acad Sci U S A 100:9584–9589.  https://doi.org/10.1073/pnas.1631069100 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nathanailides C, Kokokiris L, Karipoglou C, Kanlis G, Logothetis P, Mittakos I, Lenas D (2013) Muscle aerobic capacity and filleting yield of farmed fish species in the Mediterranean Sea. J Agric Sci Technol B 3:685–688Google Scholar
  25. Oliveira C, Sánchez-Vázquez FJ (2010) Reproduction rhythms in fish. In: Kulczykowska E, Popek W, Kapoor BG, (Eds.) Biological Clock in Fish, CRC Press, Taylor & Francis, Science Publishers, Enfield. pp 185–215.  https://doi.org/10.1201/b10170-10
  26. Oliveira C, Ortega A, López-Olmeda JF, Vera LM, Sánchez-Vázquez FJ (2007) Inflence of constant light and darkness, light intensity, and light spectrum on plasma melatonin rhythms in Senegal sole. Chronobiol Int 24:615–627.  https://doi.org/10.1080/07420520701534657 CrossRefPubMedGoogle Scholar
  27. Oliveira C, Dinis MT, Soares F, Cabrita E, Pousão-Ferreira P, Sánchez-Vázquez FJ (2009a) Lunar and daily spawning rhythms of Senegal sole (Solea senegalensis). J Fish Biol 75:61–74.  https://doi.org/10.1111/j.1095-8649.2009.02263.x CrossRefPubMedGoogle Scholar
  28. Oliveira C, Garcia EM, López-Olmeda JF, Sánchez-Vázquez FJ (2009b) Daily and circadian melatonin release in vitro by the pineal organ of two nocturnal teleost species: Senegal sole (Solea senegalensis) and tench (Tinca tinca). Comp Biochem Physiol A 153:297–302.  https://doi.org/10.1016/j.cbpa.2009.03.001 CrossRefGoogle Scholar
  29. Oliveira C, Neil DJ, Pousão-Ferreira P, Sánchez-Vázquez FJ (2010) Influence of the lunar cycle on plasma melatonin, vitellogenin and sexual steroids rhythms in Senegal sole, Solea senagalensis. Aquaculture 306:343–347.  https://doi.org/10.1016/j.aquaculture.2010.05.003 CrossRefGoogle Scholar
  30. Oliveira C, Mañanós E, Ramos J, Sánchez-Vázquez FJ (2011) Impact of photoperiod manipulation on day/night changes in melatonin, sex steroids and vitellogenin plasma levels and spawning rhythms in Senegal sole, Solea senegalensis. Comp Biochem Physiol A 159:291–295.  https://doi.org/10.1016/j.cbpa.2011.03.025 CrossRefGoogle Scholar
  31. Pardini L, Kaeffer B (2006) Feeding and circadian clocks. Reprod Nutr Dev 46:463–480.  https://doi.org/10.1051/rnd:2006032 CrossRefPubMedGoogle Scholar
  32. Saavedra M, Grade A, Candeias-Mendes A, Pereira TG, Teixeira B, Yúfera M, Conceição LEC, Mendes R, Pousão-Ferreira P (2016) Different dietary protein levels affect meagre (Argyrosomus regius) larval survival and muscle cellularity. Aquaculture 450:89–94.  https://doi.org/10.1016/j.aquaculture.2015.07.004 CrossRefGoogle Scholar
  33. Sánchez-Vázquez FJ, Madrid JA, Zamora S, Tabata M (1997) Feeding entrainment of locomotor activity rhythms in the goldfish is mediated by a feeding-entrainable circadian oscillator. J Comp Physiol A 181:121–132.  https://doi.org/10.1007/s003590050099 CrossRefGoogle Scholar
  34. Schiavone R, Zilli L, Storelli C, Vilella S (2012) Changes in hormonal profile, gonads and sperm quality of Argyrosomus regius (Pisces, Scianidae) during the first sexual differentiation and maturation. Theriogenology 77:888–898.  https://doi.org/10.1016/j.theriogenology.2011.09.014 CrossRefPubMedGoogle Scholar
  35. Skulstad OF, Taylor J, Davie A et al (2013) Effects of light regime on diurnal plasma melatonin levels and vertical distribution in farmed Atlantic cod (Gadus morhua L.) Aquaculture 414–415:280–287.  https://doi.org/10.1016/j.aquaculture.2013.08.007 CrossRefGoogle Scholar
  36. Vera LM, López-Olmeda JF, Bayarri MJ, Madrid JA, Sánchez-Vázquez FJ (2005) Influence of light intensity on plasma melatonin and locomotor activity rhythms in tench. Chronobiol Int 22:67–78.  https://doi.org/10.1081/CBI-200038157 CrossRefPubMedGoogle Scholar
  37. Vera LM, Oliveira C, López-Olmeda JF, Ramos J, Mañanós E, Madrid JA, Sánchez-Vázquez FJ (2007) Seasonal and daily plasma melatonin rhythms and reproduction in senegal sole kept under natural photoperiod and natural or controlled water temperature. J Pineal Res 43:50–55.  https://doi.org/10.1111/j.1600-079X.2007.00442.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Catarina C. V. Oliveira
    • 1
  • Filipe Figueiredo
    • 1
    • 2
  • Florbela Soares
    • 3
  • Wilson Pinto
    • 4
  • Maria Teresa Dinis
    • 1
  1. 1.CCMAR, Universidade do AlgarveFaroPortugal
  2. 2.Norwegian College of Fishery ScienceUiT The Arctic University of NorwayTromsøNorway
  3. 3.IPMAOlhãoPortugal
  4. 4.SPAROS, LdaOlhãoPortugal

Personalised recommendations