Melatonin effects on food intake and activity rhythms in two fish species with different activity patterns: Diurnal (goldfish) and nocturnal (tench)

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Abstract

Melatonin has several known physiological functions, the main one being synchronization of daily and seasonal rhythms. In addition, melatonin has been reported to influence food intake and behavioral rhythms with varying results depending on the species. The aim of this research was to evaluate the effects of intraperitoneal melatonin injection on food intake and locomotor activity in two different fish species: goldfish (diurnal) and tench (nocturnal), under different light regimes: constant light (LL) conditions or LD 12:12, with melatonin administration at mid-light (ML), mid-dark (MD), and after a 1-h light pulse at MD. In addition to these acute tests, in the case of goldfish we also investigated the effects of daily melatonin administration for 1 week. Our results indicated that acute melatonin administration significantly decreased goldfish food intake (16–52% inhibition, depending on the light regime) and locomotor activity (55–100%), with the chronic treatment inducing a similar total food intake inhibition that persisted for 7 days. In tench, a nocturnal fish species, acute melatonin administration at MD and ML reduced food intake (37% and 29%, respectively), while locomotor activity was not affected at MD and slightly increased at ML. Taken together, these results indicated that melatonin reduced food intake in both species, while its effects on locomotor activity depended on the time of administration (light or dark phase) and the activity patterns of the species.

Introduction

The role of melatonin as a chemical signal for darkness that synchronizes biological rhythms is well known (Reiter, 1993). In mammals such as the Siberian hamster, the photoperiod induces seasonal changes in energy balance and body weight via melatonin secreted by the pineal gland (Morgan et al., 2003). Melatonin is also involved in the annual rhythm of feeding behavior in the blue fox, as melatonin chronic administration modifies the seasonal pattern of food intake in this species (Nieminen et al., 2004). Indeed, melatonin has been found in the gastrointestinal tissue (GIT) of all vertebrates studied (Bubenik, 2002), although the main source of plasma melatonin is the pineal. GIT melatonin has been suggested to play a local role, regulating bicarbonate secretion by the intestinal mucosa (Sjöblom and Flemström, 2003); and also enhancing the release of gastrin and exocrine pancreatic enzymes (Jaworek et al., 2005). Furthermore, exogenous melatonin administration has been shown to have specific effects on a number of animal behaviors, including food intake regulation, albeit data are still scarce compared with other peptides and hormones whose involvement in feeding regulation is well established (Lin et al., 2000, Jensen, 2001).

The effects of melatonin may differ depending on the animal's daily living habits. The indole has been shown to decrease total food intake in many diurnal species of vertebrates (Bermúdez et al., 1983, Bubenik and Pang, 1994, Angers et al., 2003). In the rat, a nocturnal species, there is conflicting evidence concerning the effects of melatonin on food intake, as this molecule has been reported to reduce feeding (Ishibashi et al., 1966), to have no effect (Dark et al., 1980, Wolden-Hanson et al., 2000), and even to increase food consumption (Shaji and Kulkarni, 1998, Angers et al., 2003). In the case of fish, the possible differences in melatonin action in diurnal versus nocturnal species have not yet been determined.

Aside from feeding, melatonin is also known to affect locomotor activity. Thus, it reduces the activity of all diurnal species so far evaluated (Bermúdez et al., 1983, Murakami et al., 2001, Zhdanova et al., 2001, Zhdanova et al., 2002). In nocturnal species, melatonin did not seem to influence locomotor activity in owl (Murakami et al., 2001), whereas it slightly increased that of rats (Wolden-Hanson et al., 2000).

Although several studies have addressed the effects of melatonin on feeding behavior and locomotor activity in a few rodents, the relationship between them is still unclear. Furthermore, the differential effects of melatonin on fish with different activity patterns (diurnal vs. nocturnal) have still to be tested.

Thus, the aim of this research was to evaluate the effects of both acute and daily melatonin administration on food intake and activity rhythms in two fish species with opposite locomotor activity patterns, the goldfish (Carassius auratus), a fish with mostly diurnal activity (Iigo and Tabata, 1996); and the tench (Tinca tinca), a strictly nocturnal fish (Herrero et al., 2003).

Section snippets

Animals and housing

Goldfish (C. auratus) were obtained from a local dealer (Jumipez, S.A., Murcia, Spain), and had an initial body mass of 73 ± 4 g (mean ± S.E.M.). Tench (T. tinca) were obtained from the aquaculture centre “Las Vegas del Guadiana” (Badajoz, Spain), and had an initial body mass of 90 ± 7 g (mean ± S.E.M.). Animals were reared at the facilities of the University of Murcia, in special rooms or chronolabs, under constant temperature and controlled photoperiod conditions. Fish were kept in 60-l tanks, well

Results

In goldfish, melatonin reduced food intake in all experimental groups regardless the lighting conditions (Fig. 1). Food intake variations are represented as the difference between previous food intake (base line) and the actual value recorded during acute treatment. Surprisingly, vehicle administration had opposite effects, as it increased food intake in ML and MD groups, while decreasing that of MD+L and LL groups. Average daily food intake for groups under LD and LL conditions did not change

Discussion

Melatonin administration had different effects on feeding and locomotor activity depending on the activity pattern of the fish species investigated. In goldfish, a mostly diurnal fish, melatonin inhibited both food intake and locomotor activity irrespective of the light regime used. In a strict nocturnal fish like tench, on the other hand, melatonin injection reduced food intake at MD and ML, but locomotor activity was not affected at MD, and a slight activity increase was detected at ML.

Acknowledgments

This work has been supported by project AGL 2001-0593-C03-01 of the Spanish Ministry of Science and Technology (MCYT) granted to FJSV. The authors also wish to thank Dr. Imanol Martínez for his revision of the manuscript and valuable comments, and Dr. M.J. Bayarri, L.M. Vera and H. Hisano for their help with the experimental procedure. Fish were reared and manipulated following the Spanish legislation on Animal Welfare and Laboratory Practices.

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