High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus auratus)

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Abstract

Arginine vasotocin (AVT) and isotocin (IT) levels in plasma and pituitary, and melatonin (MEL) levels in plasma were determined in gilthead sea bream (Sparus auratus) subjected to two different types of stress: i) high density (HD) and ii) food deprivation (NF: non-fed). Fishes were randomly assigned to one of 4 treatments that lasted for 14 days: 1) fed fish under normal low density (ND, 4 kg m 3); 2) non-fed (NF) fish under ND; 3) fed fish under high density (HD, 70 kg m 3); and 4) non-fed fish under HD. Ten fish from each tank were anaesthetized, weighed and plasma and pituitary samples were taken. Plasma and pituitary AVT and IT content were determined by HPLC, while plasma MEL was assayed by RIA. Plasma AVT and IT values were enhanced in all fish kept at high density. The response of AVT was much stronger than that of IT. The highest pituitary AVT and IT levels were shown in NF fish kept at normal density. The significantly higher plasma MEL levels were measured in fed fish kept at HD. These results suggest a role of AVT, IT and MEL in response of sea bream to a common stress factor, high density. Although food deprivation does not influence AVT and IT plasma levels, it seems to affect hypothalamic synthesis of nonapeptides. Further studies are required to elucidate the complex role of AVT, IT and MEL in the sea bream's response to different stress stimuli.

Introduction

In teleosts, arginine vasotocin (AVT) and isotocin (IT) are synthetized in the hypothalamic magnocellular and parvocellular neurons of the preoptic nucleus (NPO), stored in the nerve terminal of these neurons at the pars nervosa of the hypophysis and released into the blood after appropriate stimuli. AVT and IT may act, either locally in the central nervous system (CNS) as neurotransmitters and/or neuromodulators, or in the peripheral target organs as hormones. In teleosts, a role of AVT in different physiological processes, such as behaviour, metabolism, reproduction, osmoregulation, etc. is well documented (Balment et al., 2006, Kulczykowska, 2007). There is also some evidence of a role of AVT and IT in stress response of teleosts. Studies in goldfish (Carassius auratus) show that AVT and IT stimulate cortisol secretion and suggest that both nonapeptides possess corticotropin-releasing factor (CRF) activity (Fryer and Leung, 1982). In Oncorhynchus mykiss, CRF and AVT synergize to stimulate adrenocorticotropin (ACTH) release (Baker et al., 1996, Pierson et al., 1996). In O. mykiss, acute confinement stress enhances AVT expression in the preoptic nucleus (Gilchriest et al., 2000) and disturbance stress increases plasma AVT, but not IT, in the same species (Kulczykowska, 2001). Recently, a similar activation of AVT expression in NPO following a single acute confinement stress has been observed in Platichthys flesus (Balment et al., 2006). IT appears to be involved in the response of female sticklebacks to a specific stressful stimuli, i.e. fish stocking density (Kleszczyńska and Kulczykowska, 2006).

The main pineal indole melatonin (N-acetyl-5-methoxytryptamine: MEL), is a pleiotropic hormone influencing many physiological processes and behaviours in vertebrates, including fish (Ekström and Meissl, 1997, Kulczykowska, 2002, Dubocovich and Markowska, 2005). An effect of stress on plasma MEL levels seems to be dependent on the type of stress stimuli (Relkin, 1989, Kulczykowska, 2001, Larson et al., 2004). However, the mechanism of MEL regulation in response to stress is not clear. It has been proposed in O. mykiss, that MEL synthesis is impaired by elevated AVT in circulation or in vasotocinergic nerve fibers projecting to the pineal organ (Kulczykowska; 2001). On the other hand, in many vertebrate species, MEL appears to be involved in the process of feeding and digesting (Harlow and Weekley, 1986, Sjöblom, 2005). The small intestine is probably an important source of extrapineal and extraretinal MEL, also in fish (Bubenik, 2002, Kulczykowska et al., 2006), and as such, a site of regulation of MEL synthesis.

The aim of the present study was to determine the response of AVT, IT and MEL in S. auratus subjected to two different types of stress: i) high density (HD) and ii) food deprivation (NF: non-fed) and explore the potential relationship between hormones. Fish were assigned to one of four treatments that lasted 14 days: 1) fed fish under normal low density (ND, 4 kg m 3), 2) non-fed fish under ND 3) fed fish under high density (HD, 70 kg m 3) and 4) non-fed fish under HD. We selected these factors because sea bream are exposed to both during aquaculture management, and there is evidence that they activate the stress response in S. auratus ( Arends et al., 1999, Montero et al., 1999, Rotllant et al., 2001, Sangiao-Alvarellos et al., 2005).

Section snippets

Animals and experimental conditions

Immature S. auratus (200–250 g body mass) were provided by Planta de Cultivos Marinos (CASEM, Universidad de Cadiz, Puerto Real, Cádiz, Spain) and transferred to the laboratories at Faculty of Marine Science (Puerto Real, Cádiz). Animals were acclimated to SW (38 p.p.t. salinity) in 300 L aquaria in an open system for at least 2 weeks. During the experiment (May 2005), fish were maintained under natural photoperiod and constant temperature (18 °C). Fish were fed once a day with commercial dry

Results

Values of plasma parameters are shown in Table 1. Under HD conditions, plasma cortisol levels increased significantly in both fed and food deprived fish, but an effect was more pronounced in NF group. Plasma glucose increased significantly in all fish kept at HD. Plasma lactate decreased in fed fish under HD and food deprived fish under ND. Proteins and triglycerides levels decreased in response to density and feeding conditions and showed the lowest values in food deprived fish kept at HD.

Discussion

High density (HD) and food deprivation (NF) are two kinds of stressors frequently used to study stress system in teleosts, including S. auratus (Barton and Iwama, 1991, Wendelaar Bonga, 1997, Sangiao-Alvarellos et al., 2005). This is the first study of AVT, IT and MEL responses in S. auratus subjected to one (HD or NF) or two combined stressors (HD plus NF). Our results on plasma cortisol, glucose, lactate and protein concentrations agreed with those reported previously for S. auratus exposed

Acknowledgements

This study was partly supported by grant BFU2004-04439-C02-01B (Ministerio de Educación y Ciencia and FEDER, Spain) to J.M.M. The authors wish to thank Planta de Cultivos Marinos (CASEM, Universidad de Cádiz, Puerto Real, Cádiz, Spain) for providing experimental fish. Dr. G. Martinez-Rodriguez and Dr. E. Kulczykowska were supported by the Consejo Superior de Investigaciones Científicas Project 2004PL0019 and the Polish Academy of Sciences travel grants.

References (40)

  • MoonsL. et al.

    Autoradiographic localization of binding sites for vasotocin in the brain and pituitary of sea bass (Dicentrarchus labrax)

    Neurosci. Lett.

    (1989)
  • RotllantJ. et al.

    Pituitary and interrenal function in gilthead sea bream (Sparus aurata L., Teleostei) after handling and confinement stress

    Gen. Comp. Endocrinol.

    (2001)
  • WarneJ.M. et al.

    Neurohypophysial hormones and renal function in fish and mammals

    Comp. Biochem. Physiol.

    (2002)
  • ArendsR.J. et al.

    The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement

    J. Endocrinol.

    (1999)
  • BubenikG.A.

    Gastrointestinal melatonin: localization, function, and clinical relevance

    Dig. Dis. Sci.

    (2002)
  • DubocovichM.L. et al.

    Functional MT1 and MT2 melatonin receptors in mammals

    Endocrine

    (2005)
  • EkströmP. et al.

    The pineal organ of teleost fishes

    Rev. Fish Biol. Fish.

    (1997)
  • GilchriestB.J. et al.

    The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss)

    J. Neuroendocrinol.

    (2000)
  • GuibboliniM.E. et al.

    Neurohypophysial hormone receptors and second messengers in trout hepatocytes

    J. Endocrinol.

    (2000)
  • HarlowH.J. et al.

    Effect of melatonin on the force of spontaneous contractions of in vitro rat small and large intestine

    J. Pineal Res.

    (1986)
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