Mitsuo Tabata

Demand feeding and locomotor circadian rhythms in the goldfish, Carassius auratus: Dual and independent phasing

In contrast to the common diurnal and nocturnal ways of life, some fish species have been shown to have a dual phasing behaviour. Therefore, the daily pattern of behaviour is not always rigidly confined to the light or dark phase and a diurnal fish may become nocturnal and vice versa. In the present study, the locomotor and feeding activities of single goldfish were simultaneously investigated to examine the existence of such dual behaviour. Nineteen goldfish weighing 97.2 g on average were placed individually in 35-1 glass tanks equipped with an infrared sensor and a newly developed self-feeding device. Fish were exposed to a light:dark (LD) 12:12 h cycle, constant darkness (DD), and 45:45 min LD pulses to study endogenous rhythmicity. Under LD 12:12, the daily pattern of behaviour differed between individual fish; some goldfish were diurnal and others were nocturnal. Furthermore, some of them displayed an extraordinary flexibility in phasing because they were light active but dark feeding, and vice versa. Generally, goldfish tended to be day active, although their feeding habits appeared equally distributed between light and dark phases. Under DD, goldfish showed free-running rhythms that averaged 25.3 +/- 1.8 h and 24.4 +/- 1.7 h for locomotor activity and feeding, respectively, but that were slightly shorter under LD pulses. These results indicate that the type of phasing of locomotor activity did not necessarily decide the feeding phase; much of this is explained by the fact that goldfish were self-fed. Flexibility in phasing and a certain degree of independence between locomotor and feeding activities could be seen as an adaptative response of the highly adaptable circadian system of fish.

Melatonin signal transduction in the goldfish, Carassius auratus.

Generation and reception of melatonin signals in the goldfish, Carassius auratus, are reviewed. The photoreceptive pineal gland of the goldfish generates circulating melatonin rhythms according to a given photoperiod under light-dark cycles and in a circadian manner under continuous dark conditions. Melatonin is also produced in the retina in a similar fashion. Melatonin produced in the pineal gland and retina is considered to act as internal zeitgeber in the brain and retina, respectively, controlling various physiological events via specific melatonin binding sites that are coupled with G protein. The goldfish exhibit clear diurnal locomotor activity rhythms under light-dark cycles and free-running rhythms under constant conditions. However, the relationship between melatonin and locomotor activity rhythms in the goldfish remains unclear. Further studies should be required to demonstrate the roles of melatonin in the circadian system in this species.

Circadian rhythms of locomotor activity in the goldfish Carassius auratus

Locomotor activities in the goldfish Carassius auratus were recorded under light-dark (LD) and constant light regimens. Under LD 12:12, all goldfish adjusted to given LD cycles. Activity patterns were classified into three types: L-type activity during the photophase (83%), LD-type activity both during the photophase and the scotophase (10%), and D-type activity during the scotophase (7%). However, these patterns were not fixed, but flexible. Under constant conditions, goldfish exhibited circadian locomotor activities: The proportions of appearance of circadian rhythms and tau values under constant darkness (DD), constant light (LL, 500 lx) and constant dim light (dimLL, 20 lx) were 57% (24.4 +/- 1.6 h, [mean +/- SE], n = 34), 57% (25.2 +/- 2.5 h, n = 35) and 67% (26.0 +/- 3.4 h, n = 10), respectively. These results indicate that the goldfish exhibit flexibility in phasing of locomotor activity rhythms under LD 12:12. In addition, the coupling between circadian clocks and locomotor activities does not seem strong, although the diel locomotor activity in the goldfish is regulated, in part, by a circadian clock. These results are discussed in context with the structure of the teleostean circadian system.

DAILY CYCLES IN PLASMA AND OCULAR MELATONIN IN DEMAND-FED SEA BASS, DICENTRARCHUS LABRAX L.

Abstract Melatonin is regarded as an internal zeitgeber, involved in the synchronization to light of the daily and seasonal rhythms of vertebrates. To date, plasma and ocular melatonin in fish have been extensively surveyed almost solely in freshwater species – with the exception of some migrating species of salmonids. In the present paper, melatonin levels of a marine species (sea bass, Dicentrarchus labrax L) were examined. In addition, the daily rhythms of the demand-feeding activity of sea bass, a fish species characterized by a dual phasing capacity (i.e. the ability to switch between diurnal and nocturnal behaviour), were investigated before sampling. Sea bass, distributed in 12 groups of four fish and kept under constant water temperature and salinity, were exposed to a 12 h light:12 h dark cycle (200:0 lx, lights on at 0800 hours). After 4 weeks recording, the animals were killed at 0900, 1200, 1400, 1600, 1900, 2100, 2400, 0200, 0400, 0700 and 0900 hours. Actograms of demand-feeding records revealed a nocturnal feeding behaviour, with some cases of spontaneous inversions in phasing. Melatonin levels in plasma peaked in the middle of the dark phase, dropping after lights on. Melatonin in the eye, on the contrary, exhibited an inverse profile, with high levels during daytime and low levels at night. These results suggest that melatonin in the plasma and the eye may act independently on the flexible circadian system of sea bass.

Unusual responses to light and darkness of ocular melatonin in European sea bass

REGULATION by light and darkness of melatonin rhythms in the plasma and eye of the European sea bass (Dicentrarchus labrax) was studied. During light–dark cycles, plasma and ocular melatonin exhibited day-night changes with higher levels at mid-dark and at mid-light, respectively. Circulating melatonin levels were low in constant light but high in constant darkness (DD); ocular melatonin levels showed the reverse pattern. Plasma melatonin exhibited circadian rhythm for 1 cycle but the rhythm was no longer apparent on day 2. There was no circadian rhythm in ocular melatonin. Acute light exposure in DD decreased plasma melatonin but increased ocular melatonin. These results suggest that circulating melatonin may be used as a signal for darkness but ocular melatonin is used as a signal for the light phase.

Ocular Melatonin Rhythms in the Goldfish, Carassius auratus

Ocular melatonin rhythms in the goldfish were studied and compared to those in the pineal organ and plasma. Under light:dark (LD) of 12 h light:12 h dark, melatonin contents in the eye as well as the pineal organ and plasma exhibited clear day-night changes with higher levels at mid-dark than at mid-light. However, melatonin contents in the eye at mid-light and mid-dark were approximately 100 and 9 times greater than those in the pineal organ, respectively. Day-night changes of ocular melatonin persisted after pinealectomy, which abolished those in plasma melatonin under LD 12:12. Ocular melatonin contents in the pinealectomized fish at mid-light were significantly higher than those in the sham-operated control. Under constant darkness (DD), circadian melatonin rhythms were observed in the eye but damped on the 3rd day, whereas plasma melatonin rhythms generated by the pineal organ persisted for at least 3 days. Under constant light, ocular melatonin contents exhibited a significant fluctuation with a smaller amplitude than that under DD, whereas plasma melatonin remained at low levels. These results indicate the involvement of LD cycles, a circadian clock, and the pineal organ in the regulation of ocular melatonin rhythms in the goldfish.

Effects of pinealectomy and constant light exposure on day-night changes of melatonin binding sites in the goldfish brain

Effects of pinealectomy and constant light exposure on day-night changes of melatonin binding sites in the goldfish brain were examined. The density and affinity of binding sites were higher at mid-day than at mid-night in sham-pinealectomized goldfish under light-dark cycles. The rhythms disappeared after pinealectomy, or constant light exposure both of which abolish plasma melatonin rhythms. The effects of pinealectomy and constant light exposure were not additive. These results indicate that diel changes of melatonin binding sites in the goldfish brain are regulated by endogenous melatonin of pineal origin.

Photoreceptor Organs and Circadian Locomotor Activity in Fishes

It is well known that fishes have photoreceptor organs other than the lateral eyes. The dominant extraretinal photoreceptor in fish is the pineal organ. The photosensitive function of the pineal organ in fish has been demonstrated in behavioral, morphological and electrophysiological studies (see review: Kavaliers, 1979b, 1980c; Tamura and Hanyu, 1980; Meissl and Dodt, 1981). There is evidence that pineal photoreception is involved in the control of circadian rhythmicity of locomotor activity (Kavaliers, 1979a, b, 1980a, b, c; Garg and Sundararaj, 1986; Tabata, 1986; Tabata et al., 1991), melatonin secretion and NAT activity (Falcon et al., Zachmann et al.; this volume).