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Circadian Rhythms in Fish

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Abstract

Circadian rhythms play a critical role in fish development and daily activities. Although a major circadian "master" clock, like the SCN of mammals, has not yet been identified in fish, indirect evidence suggests that a light-entrainable oscillator is present in fish brain. Furthermore, the structural and functional design of fish circadian systems is remarkably complicated. Photosensitive CNS-related clock organs (the pineal gland and retina), peripheral photosensitive tissues with autonomic circadian clocks, and presumed food- or temperature-entrainable circadian oscillator(s) all make for complex circadian machinery that must remain well coordinated and still be able to ensure physiological adaptation to a periodically changing environment. Such a multilevel structure of partially independent oscillators may explain the high interspecies variability observed in piscine circadian systems and substantial individual plasticity in fish behaviour and physiology. Studying these features will continue to contribute to a better understanding of the principal mechanisms involved in circadian clock functions. Data accumulated so far show that rest in fish has fundamental similarities to the behavioural manifestations of sleep in higher vertebrates. Analogous to sleep in mammals, fish show a compensatory rest rebound, reducing locomotor activity and increasing arousal thresholds after a period of rest deprivation, suggesting that fish exert a homeostatic control on rest behaviour. Furthermore, rest in fish is regulated by the circadian system, because periodic reduction in locomotor activity and increase in arousal threshold are maintained in constant darkness and occur during the subjective night. These observations, together with the hypnotic effects of melatonin and sleep-inducing agents of the benzodiazepine and barbiturate families, indicate that rest behaviour in fish can be considered a sleeplike state. Studying sleep in fish may prove to be very productive in deciphering both the enigmatic function and the physiological mechanisms of sleep.
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... Importantly, the ability for external cues to entrain biological clocks also means that circadian rhythms are inherently susceptible to dysregulation, for example due to chemical exposure (Rhee et al., 2014). Hence, the monitoring of circadian rhythms in fish has become an important tool for fish behavioural ecotoxicology that is contributing towards our understanding of how chemical stressors in the aquatic environment can affect non-target species (Melvin, 2017;Zhdanova & Reebs, 2006). ...
... sunlight and temperature) called zeitgebers (Idda et al., 2012). Zeitgebers play an important role within different intrinsic periods, that are time periods occurring during the 24 hour cycle (Zhdanova & Reebs, 2006). Each intrinsic period is caused by the adjustment of the different molecules within the oscillation phase. ...
... The oscillation phase is a process that can be either shorter or longer than the 24 hour cycle and is synchronized with light (Saini et al., 2019). This phase can then eventually clash with the environmental cycle until a relationship is achieved (Idda et al., 2012;Zhdanova & Reebs, 2006). Additionally, the utilisation of biological clocks for scientific techniques has changed over the years, with applications such as genetic and molecular analyses developed to conduct studies involving fish (Idda et al., 2012;Zhdanova & Reebs, 2006). ...
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Chemical pollution within the aquatic environment is an ongoing concern causing detrimental effects to the health of various fish populations around the world. Pharmaceuticals have become a key focus in many fish toxicological studies, causing significant changes to individual fish behaviour, with emerging interest in their ability to alter circadian rhythms. Circadian rhythms in fish are sensitive to changes to the surrounding environment, but few studies have characterised how pharmaceuticals such as antidepressants can influence these patterns. Our study investigated the circadian rhythms of male and female eastern mosquitofish (Gambusia holbrooki) collected from a freshwater pond in southeast Queensland. Mosquitofish were exposed with a control and different concentrations (1 μg/L, 10 μg/L and 100 μg/L) of the antidepressant duloxetine during 2 x 7 day and 2 x 24hr exposure periods. Behavioural endpoints such as average velocity, maximum velocity and average angular (turning) velocity were measured as the 'activity levels’ of fish between day-time and night-time through the aid of an infrared spectrum video recording camera. Our findings indicate male and female fish exhibited lower activity patterns when exposed to duloxetine. This was highlighted for the average velocity and average angular velocity as these endpoints were an apparent inverse to each other during the day and night. Additionally, female circadian rhythms were identified to be less pronounced to those in males due to the requirement of greater nutrient intake for different ecological processes. Our study indicates the need to explore further effects of other pharmaceutical contaminants, particularly antidepressants at low concentrations found within the aquatic environment to understand their potential risks to normal circadian processes in fish.
... The physiology of fish is influenced by environmental factors that change over time, such as light intensity, temperature, and food availability, among others (Hurd et al., 1998;Vera et al., 2006;Cowan et al., 2017). These changes are periodic and repetitive, meaning fish can detect these patterns and adjust their physiology appropriately, allowing them to adapt to their environment (Zhdanova and Reebs, 2005). This adaptation is achieved through external signals from the environment and collecting internal information (hormones, metabolites, enzymes) to generate physiological changes that benefit the fish during daily activities (Cymborowski, 2010). ...
... We observed a decrease in the activity of most enzymes measured in the liver during the day, suggesting reduced metabolism in the afternoon (13:00-19:00), a reduction that is independent of the food supplied in the morning hours, since no significant differences in the fed and fasted groups were detected. The liver enzyme results are probably regulated by circadian rhythms, and although we did not perform measurements in a 24 h-cycle or quantify circadian markers (bmal, clock, cry, per) (Patiño et al., 2011), the participation of circadian rhythms at the hepatic level has been widely described in mammals (Tahara and Shibata, 2016) and to a lesser extent in fish (Zhdanova and Reebs, 2005;Fujisawa et al., 2016) with patterns that are even independent of the environment (Vollmers et al., 2009;Costa et al., 2016). Additionally, the food delivered in the morning affected liver glucose and glycogen levels, with an unclear pattern for glucose but a clear increase in glycogen levels as the hours of the day pass. ...
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Eleginops maclovinus is a native species with potential for Chilean aquaculture. Understanding the variations between the post-prandial and fasted metabolic responses can contribute to improving the aquaculture of this species. This study aimed to characterize variations in intermediate metabolism during the course of the day in the liver, serum, and gills of fed and unfed fish. For this, 72 fish were assigned to two experimental groups, “fed” and “fasted”. The first group was fed “ad libitum” at 8.30, while the fasted group was not fed for 24 h. Samples were taken from both groups at 9:00, and every 2 h: 11:00, 13:00, 15:00, 17:00, and 19:00. In the fed group, food spent a long time in the gastrointestinal tract, with a large increase in stomach size and without evidence of complete emptying of the stomach at 19:00 (10.5 h post-feeding). In serum, the levels of amino acids, glucose, and triglycerides presented significant differences with peak levels at different times of day in the fed group. The cortisol in the fasted group presented a diurnal pattern with high levels during the morning and very low levels after 13:00, while in the fed group, the high cortisol variability did not allow a clear pattern to be established. In the liver, the effect of time on the enzymatic activity of the intermediary metabolism was greater compared to the effect of feeding. In the liver, enzyme activity decreased at later hours of the day, while glycogen levels increased at later hours of the day in both groups: but its levels were higher in the fed group. In gills, as well as in the liver, time had a greater effect than feeding on intermediate metabolism, since feeding only had a significant effect on the levels of hexokinase, lactate, and amino acids, suggesting an effect on carbohydrate metabolism. Meanwhile, time significantly affected the levels of Na⁺, K⁺-ATPase, glutamate dehydrogenase, aspartate aminotransferase, amino acids, and proteins, suggesting an effect on amino acid metabolism. In conclusion, the intermediate metabolism of E. maclovinus presents variations according to the time of day, with an increased metabolism during the morning and decreased metabolism as the day progresses, especially at the hepatic level. The gill tissue, despite not being a metabolic organ, presents feeding-dependent variations in its metabolism. Additional studies will be required to corroborate if coordinating a feeding strategy during the first hours of the day when metabolism is greater would improve the growth of E. maclovinus.
... www.nature.com/scientificreports/ physiological parameters 3,70 . These rhythms are under the control of different environmental cues, with the light being the strongest of these synchronizers. ...
... These rhythms are under the control of different environmental cues, with the light being the strongest of these synchronizers. Other environmental parameters changing daily or annually, including temperature and food availability, are also critical 70 . The main characteristic of these circadian rhythms is the persistence of their oscillations for a certain period of time, even in the absence of these environmental cues, by being driven by a circadian clock 3 . ...
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Melatonin is considered as the time-keeping hormone acting on important physiological functions of teleosts. While the influence of melatonin on reproduction and development is well described, its potential role on immune functions has little been considered. In order to better define an immune modulation by the melatonin hormone, we hypothesized that natural variations of photoperiod and subsequent changes in melatonin release profile may act on immune status of pikeperch. Therefore, we investigated during 70 days the effects of two photoperiod regimes simulating the fall and spring in western Europe, on pikeperch physiological and immune responses. Samples were collected at 04:00 and 15:00 at days 1, 37 and 70. Growth, plasma melatonin levels, innate immune markers and expression of immune-relevant genes in head kidney tissue were assessed. While growth and stress level were not affected by the seasonal simulated photoperiods, nocturnal levels of plasma melatonin were photoperiod-dependent. Innate immune markers, including lysozyme, complement, peroxidase and phagocytic activities, were stimulated by the fall-simulated photoperiod and a significant correlation was made with plasma melatonin. In addition to bring the first evidence of changes in fish immunocompetence related to photoperiod, our results provide an additional indication supporting the immunomodulatory action of melatonin in teleosts.
... Time-keeping systems (i.e., circadian clocks) have evolved since the most primitive forms of life to cope with natural cycles and anticipate periodic events (1). In fish, as in other vertebrates, most behavioral and physiological processes exhibit rhythms, which are driven by molecular clocks made up of transcriptional/translational loops of several clock genes (per, clock, bmal, cry, ror, and reverb) (2,3). ...
... Studies in several teleost provide well-founded data about the distribution of melatonin binding sites in wide range of body tissues (47)(48)(49)(50). Therefore, this hormone can be involved in multiple physiological processes, most of them displaying daily and/or seasonal rhythms, such as those of locomotor activity, skin pigmentation, food intake, osmoregulation, growth and reproduction [for reviews (3,4,51,52)]. Thus, the melatoninergic output is part of the time-keeping system and enable the fish to synchronize with the closest environment (51). ...
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In this article we introduce the concept of biological rhythms in fish welfare and critically discuss a neglected aspect: time-dependent issues. First we should consider that fish, like most living organisms, posses a clock that drives rhythmic biological functions. Therefore, fish stress responses are strongly affected by the time of stressor exposure (e.g. day/night) according to their daily pattern of behavior (diurnal/nocturnal). Furthermore, drugs affect fish differently depending of time of administration. For instance, commonly used substances such as anesthetics may have strikingly different effects depending on the time of day. MS-222 -the most widely used fish anesthetics- has fastest effects and higher toxicity when applied during daytime, but it is much less toxic at night. Surprisingly, no attention has been paid to this time-dependent factor when establishing dosages and protocols for fish anesthesia and euthanasia. In summary, there is a need to take into account properly the role of biological rhythms when discussing fish welfare issues and regulations by the Institutional Animal Care and Use Committee (IACUC).
... It exists in most life forms, from unicellular bacteria to higher organisms [93]. Although the basic regulatory mechanisms and functions follow the same general design, the conservation of expression of genes involved in the circadian rhythm, throughout the kingdom, is limited [94]. Here, transcriptomic and analysis showed that the core regulators of gene expression in the XX and XY brain, involved in the circadian rhythm, were altered by E 2treatment in both sexes in torafugu. ...
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Background As the critical tissue of the central nervous system, the brain has been found to be involved in gonad development. Previous studies have suggested that gonadal fate may be affected by the brain. Identifying brain-specific molecular changes that occur during estrodiol-17β (E2) -induced feminization is crucial to our understanding of the molecular control of sex differentiation by the brains of fish. Results In this study, the differential transcriptomic responses of the Takifugu rubripes larvae brain were compared after E2 treatment for 55 days. Our results showed that 514 genes were differentially expressed between E2-treated-XX (E-XX) and Control-XX (C-XX) T. rubripes, while 362 genes were differentially expressed between E2-treated-XY (E-XY) and Control-XY (C-XY). For example, the expression of cyp19a1b, gnrh1 and pgr was significantly up-regulated, while st, sl, tshβ, prl and pit-1, which belong to the growth hormone/prolactin family, were significantly down-regulated after E2 treatment, in both sexes. The arntl1, bhlbe, nr1d2, per1b, per3, cry1, cipc and ciart genes, which are involved in the circadian rhythm, were also found to be altered. Differentially expressed genes (DEGs), which were identified between E-XX and C-XX, were significantly enriched in neuroactive ligand-receptor interaction, arachidonic acid metabolism, cytokine-cytokine receptor interaction and the calcium signaling pathway. The DEGs that were identified between E-XY and C-XY were significantly enriched in tyrosine metabolism, phenylalanine metabolism, arachidonic acid metabolism and linoleic acid metabolism. Conclusion A number of genes and pathways were identified in the brain of E2-treated T. rubripes larvae by RNA-seq. It provided the opportunity for further study on the possible involvement of networks in the brain-pituitary-gonadal axis in sex differentiation in T. rubripes.
... The circadian system is responsible for the temporal organization of physiological functions that involve cycles of hormonal activity, such as melatonin and cortisol, especially every 24 h (Isorna et al. 2017), whose signaling of metabolic pathways precedes the natural events of environmental change, such as lighting, temperature, and food availability (Zhdanova and Reebs 2005). In addition to participating in circadian clocks, melatonin neutralizes free radicals and increases the activity of antioxidant enzymes, such as GPx, SOD, and CAT (Albarrán et al. 2001;Prokkola and Nikinmaa 2018;Sánchez-Vázquez et al. 2019;Tomás-Zapico and Coto-Montes 2005), and decreases the secretion of cortisol (Sánchez-Vázquez et al. 2019), which also affects the pathways of energy metabolism throughout the circadian cycle (Isorna et al. 2017). ...
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Subtropical fish are exposed to seasonal variations in temperature that impose a set of adaptations on their metabolism necessary for the maintenance of homeostasis. In this study, we addressed the effects of temperature variation on the metabolism of Astyanax lacustris, a species of freshwater fish common in the subtropical region of Brazil. Biomarkers of carbohydrate and protein metabolism, antioxidant defense, and oxidative damage were evaluated in the liver of A. lacustris exposed to low (15 °C) and high (31 °C) temperature thermal shock, with controls at 23 °C for 2, 6, 12, 24, 48, 72, and 96 h. A high energy demand was observed during the first 48 h of exposure to 15 °C, which is necessary for metabolic adjustment at low temperatures, with an increase in glycolysis, citric acid cycle, and amino acid catabolism. In addition, at 31 °C, glucose was exported in the first 12 h of exposure, and an increase in the citric acid cycle suggested acetyl-CoA as the pathway substrate, originating from the oxidation of lipids. The antioxidant defenses did not change at 15 °C, as opposed to 31 °C, in which there were changes in several antioxidant defense markers, indicating a response to the production of ROS. However, oxidative stress was observed at both temperatures, with oxidative damage detected by lipid peroxidation at 15 °C and protein carbonylation at 31 °C.
... 28,29 Fish species have diverse mating strategies and often show diurnal or seasonal patterns in mating. 24,30 Some studies characterizing courtship and mating interactions in fish species have been conducted within mating dyads and this has allowed to tease apart the discrete mating-related behaviors in the species. 31,32 Zebrafish are small shoaling cyprinids found in stagnant to slow-flowing streams of India, Bangladesh, and Nepal. ...
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Animals communicate with each other through a variety of behavioral interactions, many of which are often complex due to the interplay of several ecological factors. Observations on dyadic interactions can help throw light on the more complex interactions observed among group living organisms and can help in understanding mechanisms of behaviors related to mating strategies, dominance hierarchies, and decision-making. This study focused on the assessment of several generally observed interactions among dyads of different sexes (female-female, male-male, and male-female) in wild zebrafish (Danio rerio). Temporal dynamics of these interactive behaviors were observed in 45 dyads across 3 time intervals of the day. We used generalized linear mixed models to investigate the effect of time, sex of dyad, and their interaction on specific behaviors. While the frequency of occurrence of some behaviors showed clear variation across time intervals of the day, these were further found to depend on the composition of the dyad. Contrary to previous reports, we found that same-sex dyads are equally aggressive and aggressive interactions did not vary temporally. Mating-associated interactions, as expected, were significantly higher in mixed-sex dyads and declined significantly from early morning to afternoon. Interestingly, we also found some mating-associated interactions in same-sex dyads. A fine line exists between social and mating-associated interactions in many organisms and so we speculate that these interactions could also be social interactions and not mating-related behavior. Our findings shed light on complex interactive behaviors among zebrafish, that are likely to be affected by time as well as sex composition of interacting individuals and thus has important implications for groups varying in sex ratios in the wild.
... The effect of the lunar cycle on reproductive behavior is pervasive throughout a diverse assemblage of fishes (Johannes 1978(Johannes , 1981Taylor 1984;Takemura et al. 2004aTakemura et al. , 2004bZhdanova and Reebs 2005). Our lunar observations of these bonefish spawning migrations were strikingly similar to the traditional ecological knowledge of the species movements at Tarawa Atoll (Johannes and Yeeting 2000). ...
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Teleost fish that form predictable spawning aggregations and undertake reproductive migrations can be particularly vulnerable to overexploitation. To support community-based management of an artisanal fishery that targets bonefish (Albula glossodonta) spawning aggregations, we used a combination of acoustic telemetry, biological sampling, and remote imagery to reveal the spatiotemporal spawning migrations of bonefish on Anaa Atoll in the Tuamotu Archipelago, French Polynesia. The spawning migrations of bonefish tracked with acoustic telemetry were restricted to the northern section of the atoll, with 99.6% of all detections at offshore spawning habitats occurring on fixed acoustic receivers adjacent to the atoll’s artisanal fish trap complex. Male bonefish undertook spawning migrations more frequently than females and these spawning migrations were common during the Austral winter and fall. The movements of bonefish spawning aggregations coincided with the lunar cycle, as a network analysis revealed an increase in network size and the diversity of habitat use within our acoustic array throughout the duration of the waning moon. Our results highlighted the need for the management of the artisanal trap fishery to prevent the overharvest of bonefish during their peak spawning periods. In response to the spatiotemporal management recommendations derived from this research, the local government established an Educational Managed Marine Area that includes the atoll’s bonefish spawning migratory corridor adjacent to Tukuhora village and a Rahui (i.e., seasonal closure) to improve the sustainability of the fishery.
... The fish resumed standard metabolic mode from resting at dawn when they increased their oxygen consumption to support energy generation. This is regulated by their circadian cycle, as the circadian clock is known to influence the metabolic responses that are crucial for the organisms to maintain their homeostasis (Zhdanova and Reebs 2006;Eckel-Mahan and Sassone-Corsi 2013;Asher and Sassone-Corsi 2015). In fact, feeding the fish according to its natural feeding habit with proper feeding practice can achieve high feeding efficiency and contribute to better growth performance. ...
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This chapter summarizes the evidence concerning physiological and behavioral rhythms in fish and discusses these in their appropriate context. The evidence for or against the endogenous nature of daily rhythms of activity in fish has been somewhat contradictory. The possibility of “innate timing mechanisms” and listing a “physiological clock” is one of the biological factors influencing migrations. The slow acceptance of the idea of innate timing mechanisms may also result from incorrectly placed emphasis concerning their ecological usefulness as mere daily regulators restricting certain activities to specific and appropriate times of day or night in the presence of strong periodic factors of the environment that could be sufficient to directly cause, or properly time, these activities. A more important role of the daily rhythms lies in their basic involvement in photoperiodic induction phenomena, photoperiodism. The chapter summarizes the available experimental evidence concerning rhythms in fish and relates these data to recently developed ideas and theories about biological rhythms in general. The chapter reviews the currently prevailing concepts concerning biological time measuring.