Environmental Cycles, Melatonin, and Circadian Control of Stress Response in Fish

Abstract

Fish have evolved a biological clock to cope with environmental cycles, so they display circadian rhythms in most physiological functions including stress response. Photoperiodic information is transduced by the pineal organ into a rhythmic secretion of melatonin, which is released into the blood circulation with high concentrations at night and low during the day. The melatonin rhythmic profile is under the control of circadian clocks in most fish (except salmonids), and it is considered as an important output of the circadian system, thus modulating most daily behavioral and physiological rhythms. Lighting conditions (intensity and spectrum) change in the underwater environment and affect fish embryo and larvae development: constant light/darkness or red lights can lead to increased malformations and mortality, whereas blue light usually results in best hatching rates and growth performance in marine fish. Many factors display daily rhythms along the hypothalamus-pituitary-interrenal (HPI) axis that controls stress response in fish, including corticotropin-releasing hormone (Crh) and its binding protein (Crhbp), proopiomelanocortin A and B (Pomca and Pomcb), and plasma cortisol, glucose, and lactate. Many of these circadian rhythms are under the control of endogenous molecular clocks, which consist of self-sustained transcriptional-translational feedback loops involving the cyclic expression of circadian clock genes ( clock, bmal, per , and cry ) which persists under constant light or darkness. Exposing fish to a stressor can result in altered rhythms of most stress indicators, such as cortisol, glucose, and lactate among others, as well as daily rhythms of most behavioral and physiological functions. In addition, crh and pomca expression profiles can be affected by other factors such as light spectrum, which strongly influence the expression profile of growth-related ( igf1a, igf2a ) genes. Additionally, the daily cycle of water temperature (warmer at day and cooler at night) is another factor that has to be considered. The response to any acute stressor is not only species dependent, but also depends on the time of the day when the stress occurs: nocturnal species show higher responses when stressed during day time, whereas diurnal fish respond stronger at night. Melatonin administration in fish has sedative effects with a reduction in locomotor activity and cortisol levels, as well as reduced liver glycogen and dopaminergic and serotonergic activities within the hypothalamus. In this paper, we are reviewing the role of environmental cycles and biological clocks on the entrainment of daily rhythms in the HPI axis and stress responses in fish.

The Effect of Orally Supplemented Melatonin on Larval Performance and Skeletal Deformities in Farmed Gilthead Seabream (Sparus aurata)

“…In the present study, the three groups of larvae (control group and two groups treated with different concentrations of melatonin) were placed under common hatchery conditions in continuous light to investigate the melatonin effect on skeletal abnormalities and growth rate in gilthead seabream. In teleosts, the melatonin synthesis reported on the pineal gland and gut has daily rhythms that adjust to the relevant photoperiod [ 14 , 15 , 16 ]. Additionally, the retinal melatonin acts as a local neuromodulator, and it is metabolized in situ.…”

“…The circadian rhythm alternation has a major role in synchronizing daily behavioral processes in fish (locomotor activity, sedation, food intake, shoaling behavior), skin pigmentation, oxygen consumption, thermoregulation, and melatonin synthesis [ 13 ]. In fish, as in mammals, melatonin is the output signal of the circadian clock, a crucial hormone produced by the pineal gland that displays daily and seasonal patterns of secretion with a peak level during the dark-phase and basal level during the photo-phase [ 14 ]. The synthesis of melatonin also occurs in the retina.…”

“…The synthesis of melatonin also occurs in the retina. Retinal melatonin acts as a local neuromodulator within the eye, and it could be metabolized in situ, which prevents retinal melatonin from being released into the blood [ 14 ]. In addition, mRNA transcripts of melatonin synthesis enzymes have been reported in the digestive tracts of several teleosts with daily rhythms that adjust to the prevalent photoperiod [ 13 , 14 , 15 , 16 ].…”

“…Retinal melatonin acts as a local neuromodulator within the eye, and it could be metabolized in situ, which prevents retinal melatonin from being released into the blood [ 14 ]. In addition, mRNA transcripts of melatonin synthesis enzymes have been reported in the digestive tracts of several teleosts with daily rhythms that adjust to the prevalent photoperiod [ 13 , 14 , 15 , 16 ]. The involvement of melatonin in larval development and growth has been demonstrated by several in vivo and in vitro studies [ 17 , 18 , 19 , 20 , 21 , 22 ] showing that melatonin stimulates cell proliferation and embryonic development in a dose-dependent manner in zebrafish [ 17 , 18 ].…”

A Susceptible Period of Photic Day-Night Rhythm Loss in Common Marmoset Social Behavior Development

“…A circadian rhythm abnormality is one of the major issues in developmental psychiatry reported in autism ( Tordjman et al, 2015 ) and bipolar disorders ( Gottlieb et al, 2019 ) characterized by social communication and emotional behavior impairments which needs further research on treatment design such as comprehensive intervention with environmental care ( Arns et al, 2013 ), diet ( Miller et al, 2015 ), home education ( Raffington et al, 2018 ), and pharmacological treatment ( Bourgeron, 2007 ). Among these considered factors, a photic day-night environmental rhythm applicable to humans and any other diurnal or nocturnal animals who form general circadian rhythms have been found pathogenesis, molecular, synaptic and neuronal mechanisms of cognition and behavior) using animal models in the field of developmental psychiatry ( Homberg et al, 2016 ; Crossland et al, 2017 ; Sánchez-Vázquez et al, 2019 ).…”