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Circadian Rhythms in Fish
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.
... "Circadian rhythm" is also among the significantly enriched GO terms in delta smelt (Hypomesus transpacificus) and inland silverside (Menidia beryllina) exposed to sublethal temperatures (Komoroske et al., 2021). Among the top DEGs include genes such as clocka, per3, nr1d2b, cry3a, and dbpa which are known to regulate circadian rhythm in fish (Zhdanova and Reebs, 2005;Amaral and Johnston, 2012;Frøland Steindal and Whitmore, 2019). These observations indicate the role of temperature as an environmental zeitgeber (time cue) that influences circadian rhythm in fish (Zhdanova and Reebs, 2005). ...
... Among the top DEGs include genes such as clocka, per3, nr1d2b, cry3a, and dbpa which are known to regulate circadian rhythm in fish (Zhdanova and Reebs, 2005;Amaral and Johnston, 2012;Frøland Steindal and Whitmore, 2019). These observations indicate the role of temperature as an environmental zeitgeber (time cue) that influences circadian rhythm in fish (Zhdanova and Reebs, 2005). Taken together, our findings suggest that during deployment in salmon cages, the physiological and molecular response strategies of ballan wrasse to environmental stimuli or stressors vary with seasonal changes in ambient temperature. ...
Thermal condition has profound influence on physiology and behaviour of ballan wrasse (Labrus bergylta), a cleaner fish commonly deployed in salmon cages to control sea lice infection. To address knowledge gaps on the species thermal biology, critical thermal limits were determined by acclimating fish (21.5 ± 3.1 g, 10.5 ± 0.4 cm) at a range of temperatures (6, 10, or 14°C) found in its natural habitat on the west coast of Scotland for one week and subjecting them to ramping temperature (~0.3°C/min) until loss of equilibrium. Critical thermal maxima (CTmax), minima (CTmin), and thermal breadth values increased with acclimation temperature. Thermal tolerance polygon was constructed and showed the intrinsic (7.9 to 16.8°C) and acquired (3.4°C and 22.8°C) thermal tolerance zones, supporting the seasonal differences in behaviour and delousing efficacy of ballan wrasse deployed in salmon farms. Gill transcriptomic profiles of ballan wrasse were performed following thermal acclimation and subsequent exposure to CTmax and CTmin. Initial acclimation resulted in unique differentially expressed genes (DEGs) and enrichment of GO terms that were almost exclusively found in each acclimation group. Transcriptome response to CTmax and CTmin also varied between acclimation groups. CTmax and CTmin shared 0% DEGs at 6°C, 43% at 10°C, and 7% at 14°C, but some overlapping GO terms. This study is the first to investigate the thermal tolerance limits of ballan wrasse and provides new data into the plasticity of thermal tolerance limits and molecular response to thermal stimuli in fish.
... Food availability is among the most critical factors determining predator movement patterns, influencing home range size, activity levels and timing (Mitchell and Powell 2004;Zhdanova and Reebs 2006). Numerous studies have demonstrated a negative correlation between predators' home range size or activity and prey density, when predators expand their range or increase activity when prey is scarce (Ferguson et al. 2009;Herfindal et al. 2005;Loveridge et al. 2009). ...
The availability and spatial distribution of prey determine the energetic costs of predators foraging and largely drive their space use, activity level and foraging timing. Consequently, predators in ecosystems with different prey availability and distribution should adjust their movement patterns to optimise their foraging success in order to maximise efficiency.
The aim of this study was to investigate the ability of a top predator, European catfish ( Silurus glanis ), to adapt its space use, temporal activity and diet patterns in environments with varying prey density and distribution and to examine the consequences for the catfish's body growth.
Catfish activity, tracked with high‐resolution acoustic telemetry positioning systems deployed in two oligotrophic lakes with limited fish prey and one eutrophic reservoir with abundant fish prey, showed clear differences in their spatial and foraging behaviour. In oligotrophic, prey‐poor lakes, catfish showed larger space use, altered diurnal activity patterns, reduced use of the open water, increased variability in inter‐ and intra‐individual space use and had a more diverse diet compared to their conspecifics in the eutrophic, prey‐rich reservoir. The reduced availability of prey in oligotrophic lakes resulted in slower catfish growth, as the adaptations could not fully compensate for the reduced abundance of prey fish.
The study showed that top predators can combine different behavioural mechanisms and individual strategies to adapt to different ecological contexts. The observed ability of catfish to adjust activity, space use and diet reflects an adaptive strategy to improve foraging efficiency and overall fitness in varying habitats. These behavioural adaptations may provide catfish with advantages over other top predators in terms of resource exploitation. Such competitive abilities are important for the catfish's success as an invasive species within Europe.
... (Sánchez-Vázquez et al. 2019), modulating in this way the circadian rhythm of animals. However, although fish hypothalamus, and in some teleost species also the pineal gland, contain circadian oscillators (Martín-Robles et al. 2012;Nisembaum et al. 2012;Vera et al. 2013), no master clock has been yet identified (Zhdanova and Reebs 2005). On the other hand, neuropeptides that maintain and modulate the main circadian oscillator clocks, appear to be conserved from invertebrates to mammals (Partch et al. 2014). ...
Neuropeptides are highly variable but widely conserved molecules, the main functions of which are the regulation and coordination of physiological processes and behaviors. They are synthesized in the nervous system and generally act on other neuronal and non‐neuronal tissues or organs. In recent years, diverse neuropeptide isoforms and their receptors have been identified in different fish species, regulating functions in the neuroendocrine (e.g., corticotropin‐releasing hormone and arginine vasotocin), immune (e.g., vasoactive intestinal polypeptide and somatostatin), digestive (e.g., neuropeptide Y), and reproductive (e.g., isotocin) systems, as well as in the commensal microbiota. Interestingly, all these processes carried out by neuropeptides are integrated into the nervous system and are manifested externally in the behavior and affective states of fish, thus having an impact on the modulation of these actions. In this sense, the monitoring of neuropeptides may represent a new approach to assess animal welfare, targeting both physiological and affective aspects in fish. Therefore, although there are many studies investigating the action of neuropeptides in a wide range of paradigms, especially in mammals, their study within a fish welfare framework is scarce. To the best of our knowledge, this is the first review that gathers and integrates up‐to‐date information on neuropeptides from an animal welfare perspective. In this review, we summarize current findings on neuropeptides in fish and discuss their possible implication in the physiological and emotional state of fish, and therefore in their welfare.
... In general, circadian rhythms are an intrinsic and natural characteristic of living organisms. The regulatory mechanisms of organisms-including biochemical, physiological, molecular, and detoxification processes-function based on circadian rhythms, which are governed by endogenous timekeeping mechanisms [52]. When the levels of respiratory gases (such as oxygen) in an organism decrease, circadian rhythms may be affected. ...
This study involved the use of a real-time online respiratory metabolism-monitoring system to examine the effects of water temperature on koi carp metabolism, focusing on the oxygen-consumption rate (OCR), carbon dioxide-excretion rate (CER), and respiratory quotient (RQ). Experiments were conducted at four temperatures: 18 °C, 22 °C, 26 °C, and 30 °C. The results showed that as the temperature increased from 18 °C to 26 °C, the OCR and CER rose significantly, indicating higher metabolic rates. At 30 °C, these indicators declined, reflecting physiological stress and reduced efficiency. The RQ showed minimal fluctuations at 22 °C, suggesting optimal metabolic stability, while at 26 °C and 30 °C, RQ fluctuations increased and rhythmicity was lost, indicating disrupted metabolic activity. Autocorrelation and self-organizing map (SOM) analyses revealed stable circadian rhythms at 18 °C and 22 °C, which were significantly disrupted at higher temperatures. These findings indicate that the optimal temperature range for koi carp is 22 °C to 26 °C, at which temperatures metabolic activity is efficient and rhythms are stable. Beyond this range, metabolism becomes disrupted. This study underscores the importance of maintaining suitable water temperatures in aquaculture to promote fish health and productivity, particularly in the context of climate change.
... Diel activity patterns can be endogenous (i.e., circadian rhythms) and are often shaped by the multifaceted trade-offs that animals must manage in response to changes in internal and external biotic conditions and abiotic factors (e.g., Aschoff 1960;Daan and Aschoff 1981;Metcalfe et al. 1998Metcalfe et al. , 1999. The optimal time to be active can depend on prey activity and availability, environmental conditions, the need to avoid predators, and/or the need to reduce competition (e.g., Nelson and Vance 1979;Metcalfe et al. 1999;Reebs 2002;Kronfeld-Schor and Dayan 2003;Zhdanova and Reebs 2006;Bosiger and McCormick 2014;Courbin et al. 2019;Tatler et al. 2021). Temperature-dependent physiological processes, body condition, seasonal changes, and on-togeny also affect animal activity (e.g., Metcalfe et al. 1998;Matern et al. 2000;Reebs 2002;Houston and McNamara 2014;Tatler et al. 2021). ...
Elasmobranchs often exhibit nocturnal or crepuscular activity, with shark diel patterns being better understood than ray diel patterns. We used accelerometry and hidden Markov models (HMMs) to classify female southern stingray (Hypanus americanus Hildebrand & Schroeder, 1928) activity states across diel periods and environmental conditions in Belize. Three state (low, medium, and high activity) HMMs were constructed for all individuals together and separately (N = 9). Combined, stingrays were most likely to be highly active at night and in low and medium activity states in the morning. However, there was individual variation in diel activity. In contrast, all stingrays consistently used shallow water (<4 m) during periods of high activity. Temperature had less influence on activity patterns, although three individuals exhibited high activity in cooler water. Generally, high stingray activity was driven by diel cycles and depth. Future research should link activity states to specific behaviours, include a larger sample size, extend tag deployment durations, and explore the impact of predator and prey dynamics on stingray activity.
... The circadian rhythm is predominantly controlled by a transcription-translation feedback loop, where the heterodimeric interactions of BMAL1 and CLOCK drive the transcription of period (PER1-3) and cryptochrome (CRY1-2) through E-box. Subsequently, the accumulation of the PER-CRY complex inhibits the activity of the CLOCK-BMAL1 heterodimer, forming a negative feedback loop (Cahill, 2002;Zhdanova and Reebs, 2006;Liu et al., 2022). In addition, AMP-activated protein kinase (AMPK) serves as a metabolic modulator that recovers energy homeostasis during metabolic stimuli. ...
... food availability) often occur with predictable likelihood over the course of the day (Alanärä and Brännäs, 1997;Bécares et al., 2015). This cyclic oscillation is generally synchronised with environmental time cues, such as the light-dark cycle determined by the 24 h period of the Earth's rotation on its axis (Zhdanova and Reebs, 2005). Environmental variables can thereby act as predictive signals for animals, allowing them to adjust their behaviour in advance and effectively cope with daily challenges. ...
... Multiple pathways involved in ultradian rhythm, water homeostasis, and protein metabolism, and meiotic cell cycle were enriched. Ultradian rhythm is important in diverse functions including growth, reproduction, and metabolism in fish (Cowan, Azpeleta, and López-Olmeda 2017;Frøland Steindal and Whitmore 2019;Sánchez-Vázquez et al. 2019;Zhdanova and Reebs 2006). Diverse metabolic processes involving amino acids were also significantly enriched, which is critical for fish growth rates (Finn and Fyhn 2010;Pelletier et al. 1994). ...
Humans have become one of the greatest evolutionary forces, and their perturbations are expected to elicit strong evolutionary responses. Accordingly, during (size) selective overharvesting of wild populations, marked phenotypic changes have been documented, while the evolutionary basis is often unresolved. Time-series collections combined with genomic tools present unique opportunities to study how evolutionary changes are manifested at the genome-wide level. Here, we take advantage of a unique temporal dataset from the overexploited Eastern Baltic cod (Gadus morhua) population that exhibited a 48% decrease in asymptotic body length over the last 25 years. A genome-wide association study revealed pronounced peaks of outliers linked to growth performance. The contributing loci showed signals of directional selection with significantly high autocovariance in the allele frequency and excessive intersections with regions of high Fst as well as genes relevant to growth and reproduction. Moreover, pattern of directional selection for ancestral haplotype of the well-known chromosomal inversions in Atlantic cod (on linkage group 12) was observed, while the double crossover (~1Mb) enharbouring the vitellogenin genes within this region showed signs of drift or balancing selection. Our results demonstrate evident response of the genome over a relatively short time frame and further underscore implications for fisheries management and conservation policy regarding the adaptive potential of marine populations.
... As observed in mammals, biological activities and behaviour are regulated by daily rhythmicity in aquatic species. A homolog of the suprachiasmatic nucleus has been found ventrally in the hypothalamus that may play a circadian role in some fish species (Zhdanova and Reebs 2005). Thermoregulation in ectotherms occurs through behaviour. ...
This review highlights recent findings on biological rhythms and discusses their implications for the management and production of domestic animals. Biological rhythms provide temporal coordination between organs and tissues in order to anticipate environmental changes, orchestrating biochemical, physiological and behavioural processes as the right process may occur at the right time. This allows animals to adapt their internal physiological functions, such as sleep-wake cycles, body temperature, hormone secretion, food intake and regulation of physical performance to environmental stimuli that constantly change. The study and evaluation of biological rhythms of various physiological parameters allows the assessment of the welfare status of animals. Alteration of biological rhythms represents an imbalance of the state of homeostasis that can be found in different management conditions.
To identify daily changes in the digestive physiology of Totoaba macdonaldi, the feed intake, activity (pepsin, trypsin, chymotrypsin, lipase, amylase, and L-aminopeptidase), and gene expression (aminopeptidase and maltase-glucoamylase) of key digestive enzymes were measured in the intestine and the pyloric caeca. Fish were fed for three weeks every four hours during the light period to apparent satiation, and samples were taken every four hours throughout a 24-h cycle under a 12:12 L:D photoperiod. The feed consumption steadily increased until the third feeding (16:00 h, ZT-8) and decreased significantly towards the end of the day. The activity of pepsin and alkaline enzymes (trypsin, chymotrypsin, lipase, amylase, and L-aminopeptidase) exhibited a pattern dependent on the presence of feed, showing a significant reduction during the hours of darkness (ZT-12 to ZT-24). Expression of the intestinal brush border enzyme (L-aminopeptidase) increased during the darkness period in anticipation of the feed ingestion associated with the subsequent light period. The cosinor analysis used to estimate the feed rhythms for all tested enzymes showed that activity in the intestine and pyloric caeca exhibited significant rhythmicity (p < 0.05). However, no rhythmicity was observed in the intestinal expression of maltase-glucoamylase. Our results demonstrate that some of the behavioral and digestive physiology features of totoaba
directly respond to rhythmicity in feeding, a finding that should be considered when establishing optimized feeding protocols.
1. The swimming activity of 6 specimens of the Pachon cave form of Astyanax mexicanus was tested with regard to its time control under various light-dark(LD)cycles and constant conditions, and it is compared to that of a river form.
2. In general, activity is entrainable by all applied LDs, but even if the amplitude of a forcing signal increases the signal energies are lower than in the river fish.
3. In case of entrainment the maximum values of surface activity correspond to the dark phases, those of bottom activity to the light phases of a LD. Flexible patterns -as often observed in the river form in the range of resonance about 24 h - are very seldom. Furthermore, disturbances of ten occur in the entrainment of one activity form, or one form runs arrhythmic while the other is still entrained.
4. The activity answers to changing environmental conditions are not as uniformly quick as in the river fish. But the system hardly needs a swing-in time to become entrained when a LD starts.
5. After transition from LD to DD (= constant darkness) the entrained rhythms disappear immediately.
6. In no LD with a period length differing from 24 h a circadian rhythm can be observed in addition to the entrained frequency.
7. These results show that the passive system of the river form has developped into an extremely passive one being unable to oscillate and thus has become simplified during regressive evolution. Concerning the circadian oscillator of the epigean ancestor, it was also subjected to regression, but it has not been completely lost. After a LD with a period length about 24 h the circadian oscillator is able to act as a stable system, clearly shown by the freerunning circadian rhythms of surface activity. But out of this range the oscillator is unable to control activity. In DD after all other LDs activity patterns are arrhythmic.
There is no information on whether the daily foraging movements of fish shoals are the result of chance, the collective will of all shoalmates, or the leadership of a few individuals. This study tested the latter possibility. Shoals of 12 golden shiners, Notemigonus crysoleucas, were trained to expect food around midday in one of the brightly lit corners of their tank. They displayed daily food-anticipatory activity by leaving the shady area of their tank and spending more and more time in the food corner up to the normal time of feeding. Past this normal time they remained in the shade, even on test days when no food was delivered. Most of these experienced individuals were then replaced by naïve ones. The resulting ratio of experienced:naïve fish could be 5:7, 3:9 or 1:11. On their own, naïve individuals would normally spend the whole day in the shade, but in all tests the experienced individual(s) were able to entrain these more numerous naïve fish out of the shade and into the brightly lit food corner at the right time of day. Entrainment was stronger in the 5:7 than in the 1:11 experiment. The test shoals never split up and were always led by the same fish, presumably the experienced individuals. These results indicate that in a strongly gregarious species, such as the golden shiner, a minority of informed individuals can lead a shoal to food, either through social facilitation of foraging movements or by eliciting following behaviour. Copyright 2000 The Association for the Study of Animal Behaviour.
We have previously shown that the testicular development of underyearling male masu salmon Oncorhynchus masou reared under a long photoperiod was accelerated by oral melatonin treatment (0.5mg melatonin/kg body weight/day), suggesting that melatonin mediates photoperiodic signaling. In this study, we further examined the effects of a disturbance in the plasma melatonin profile on gonadal development in underyearling male masu salmon by administering a higher dose of melatonin. Fish randomly selected in June were divided into two groups. They were reared under a light:dark (LD) cycle of 16:8 (lights on 04:00-20:00 hr) and fed with pellets sprayed with melatonin or vehicle twice a day at 08:30 and at 15:30 hr (7.5mg melatonin/kg body weight/day) until October. Fish were sampled on Day 0, 25, 60, 90 and 120. The plasma melatonin levels were high in the dark phase and low in the light phase in the control group, while they were constantly high with no significant change in the melatonin-treated group. Melatonin treatment had inhibitory effects on the gonadosomatic index and plasma testosterone levels. Pituitary salmon gonadotropin-releasing hormone content and luteinizing hormone content were significantly lower in the melatonin-treated group on Day 60 and 90, respectively. These results indicate that the plasma melatonin profile is important for mediating photoperiodic signals that regulate brain-pituitary-gonadal axis in underyearling precocious male masu salmon.
The threat of predation has profound and pervasive effects on prey fishes. If we begin with structure, the body shape, size, the degree and type of body armour, and the size and arrangement of spines are all subject to selection by predators. Colours that may attract mates can also make an animal conspicuous to predators, leading to seasonal changes in appearance or to colours that may be less than optimal for mate attraction. Control of seasonal colour changes is probably a physiological response to predation, as is the production of toxins and venoms. Behavioural responses to predation are very diverse and include avoiding dangerous areas, hiding at certain times of day and recognising predators and fleeing or hiding from them, as well as evasive tactics at the moment of attack.
The influence of the eyes and pineal gland on locomotor activity rhythms of channel catfish, Ictalurus punctatus, and the extent to which varying light intensity altered these activity rhythms were evaluated. Locomotor activity was measured in normal, blinded, pinealectomized, and pinealectomized-blinded channel catfish exposed to a 12:12 light/dark photoperiod of decreasing light intensities (7,500, 175, and 0.7 lx). Normal, blinded, and pinealectomized fish exhibited nocturnal activity patterns which corresponded with the exogenous photoperiod. Fish without lateral eyes and pineal gland did not entrain to the photoperiod but had arrhythmic activity patterns. Neither treatment nor light intensity affected total locomotor activity. Blinding or pinealectomy decreased the level of dark-period activity at low light intensities, but the effect of light intensity was not observed in normal and pinealectomized-blinded fish. Normal and blinded fish under constant light or constant dark exhibited arrhythmic activity. The pineal gland functions as an extraretinal light receptor in channel catfish.
The behavior of an animal, as well as its related physiological processes, is often rhythmic. An event may take place only at a certain time of day or night or season or year corresponding to certain natural external cycles. These cycles may exert varying degrees of control; their influence may be total, with the entire response dependent on the continued presence of the stimulus, or they may act as a cue, initiating, terminating, or synchronizing a particular event which is basically internally controlled. Knowledge of the relation of the external cycle to the behavior of the animal is essential to understanding the harmony between organism and environment. It allows us to predict when and where certain events are most likely to occur as well as when an animal may be predisposed to respond to a particular stimulus. In this chapter we examine, quantitatively, daily and seasonal rhythms in swimming speed and schooling of a marine pelagic migrating species, the bluefish, Pomatomus saltatrix L., held under controlled laboratory conditions.
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.