Environmental Control of the Seasonal Variations in ... - Science Direct

General and Comparative Endocrinology 106, 85–94 (1997) Article No. GC966853

Environmental Control of the Seasonal Variations in the Daily Pattern of Melatonin Synthesis in the European Hamster, Cricetus cricetus B. Vivien-Roels,*,1 B. Pitrosky,* M. Zitouni,* A. Malan,* B. Canguilhem,† D. Bonn,* and P. Pe´vet* *URA-CNRS 1332, Neurobiologie des fonctions rythmiques et saisonnie`res, Laboratoire de Zoologie, Universite´ Louis Pasteur, Strasbourg, France; and †Institut de Physiologie, URA CNRS 1332, Faculte´ de Me´decine, Universite´ Louis Pasteur, Strasbourg, France Accepted November 11, 1996

Nocturnal patterns of pineal melatonin concentrations were measured at hourly intervals in the European hamster, Cricetus cricetus, maintained under different natural or experimental environmental conditions. There were pronounced variations in the night peak of pineal melatonin both in the duration and the amplitude of the melatonin peak and in the onset and decline of melatonin synthesis. The duration of the melatonin peak increased proportionnally with increased dark period. The amplitude increased abruptly from LD 16/8 to LD 15/9 and remained constant in all other photoperiods. The onset of synthesis started 6:00 hours after the onset of darkness in LD 16/8, 15/9, and 14/10, while it started 4:00 hours after dark onset in shorter photoperiods (LD 12/12 and 10/14). This result is opposite to that observed in the rat. The decline of synthesis was delayed as darkness increased and was directly related to lights on in long photoperiods, while it was endogenous in short photoperiods. Temperature, under a long photoperiod, also seems to be implicated in the regulation of the amplitude of the melatonin peak. r 1997 Academic Press

1 To whom correspondence should be addressed at URA-CNRS 1332 ‘‘Neurobiologie des fonctions rythmiques et saisonnie`res,’’ Laboratoire de Zoologie, Universite´ Louis Pasteur, 12 rue de l’Universite´, 67000 Strasbourg, France. Fax: (33) 388.24.04.61. E-mail: [email protected].

0016-6480/97 $25.00 Copyright r 1997 by Academic Press All rights of reproduction in any form reserved.

Many species living in temperate regions use photoperiodic information to regulate their annual cycles of reproduction. Photoperiod is conveyed to the central nervous system via the daily pattern of melatonin synthesis and secretion (Goldman, 1983; Hoffmann, 1985; Reiter, 1987a; Pe´vet, 1988). Natural or experimental photoperiodic changes alter the duration of melatonin synthesis in many species (ref. in Hoffmann et al., 1985; Illnerova, 1986; Vivien-Roels et al., 1988; Pe´vet et al., 1991) and in most mammals the duration of the nocturnal peak of melatonin secretion is proportional to the duration of the dark period. Melatonin infusions into pinealectomized sheep or hamsters can reproduce the effects of either a short or a long photoperiod (Carter and Goldman, 1983; Bittman and Karsch, 1983; Pitrosky et al., 1991). These results have led to the ‘‘duration hypothesis,’’ according to which photoperiodic information is conveyed to the central nervous system by the duration of the nocturnal peak of melatonin (Bartness et al., 1983). Nevertheless, it is now increasingly evident that seasonal changes in the daily pattern of melatonin secretion are more complex than a simple change in the duration of the night peak (Pe´vet et al., 1991, 1995; Reiter, 1987b). The changes may also affect the amplitude of the melatonin rhythm or its phase with respect to the light–dark cycle (Pe´vet et al., 1995; Vivien-Roels, 1996).

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The European hamster is a seasonal breeder using photoperiodic information via the pineal gland to regulate its seasonal reproductive activity (Canguilhem et al., 1986; Masson-Pe´vet et al., 1987). Pe´vet et al. (1989) and Vivien-Roels et al. (1992) reported wide seasonal changes in both the amplitude and the duration of the day–night rhythm of melatonin concentrations in the European hamster, with a lack of day–night variations in late spring and early summer. Nevertheless, when animals are experimentally exposed to a long photoperiod (LP 16/8) at 20° for 6 weeks in summer, a small but significant increase in pineal melatonin concentration was observed at the end of the dark period (Vivien-Roels et al., 1993). Such a difference may be due to other environmental factors, such as temperature, that may influence the daily pattern of melatonin synthesis under natural conditions (Pe´vet et al., 1991; Vivien-Roels et al., 1992). Another possibility is that a very short increase in the night pineal melatonin synthesis might have remained unnoticed when animals were sacrificed every 3 or 4 hr during a 24-hr cycle (Pe´vet et al., 1989). To define more precisely the patterns of melatonin synthesis and to evaluate the impact of photoperiod and temperature on pineal activity, the variations of pineal melatonin concentrations during the night have been determined, at hourly intervals. In addition, the effects of environmental temperature and photoperiod on these daily variations have been determined.

MATERIAL AND METHODS

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ether anesthesia. Pineal glands were quickly removed, frozen in liquid nitrogen, and stored at 220°.

Experiment 1 Females (60) caught in April and maintained under natural outdoor conditions until the end of May were transferred for 6 weeks (May 28th–July 12th) under a long photoperiod (LD 16/8, lights on 04:00–20:00 hr) at three different temperatures: 10°, 20°, and 30°. Groups of 5 animals were killed respectively at 11:00, 15:00, 24:00, and 03:00 hr.

Experiment 2 Females (395) caught in April and maintained under natural outdoor conditions were transferred for 6 weeks to 15 6 1°, under various photoperiods: LD 16/8, LD 15/9, LD 14/10, LD 12/12 (from April 12th to June 03rd) or LD 10/14, LD 8/16 (from June 15th to July 29th). In all photoperiodic conditions the dark period started at 20:00 hr. Groups of 5 or 6 animals were sacrificed every hour or every 1.5 hr during darkness, the first group being killed 30 min before lights off and the last group 30 min after lights on.

Experiment 3 Females (142) were maintained under natural outdoor conditions from the time of capture in April. Groups of 5 or 6 animals were sacrificed every hour during darkness at three different times of the year: June 10th, August 3rd, and September 15th (the first groups were killed 1 hr before dusk, the last groups 1 hr after dawn).

Animals Experiment 4

The experiments reported were conducted between 1991 and 1994. Female European hamsters were caught every year in April in the countryside in the vicinity of Strasbourg, France (altitude 143 m, latitude 48° 358 N), and then maintained in individual cages in natural outdoor conditions with water and food ad libitum until study.

Females (45) were maintained outdoors under natural conditions from April to October 1994. They were then transferred for 6 weeks (October 19th–November 30th) to 15°C under a long photoperiod (LD 16/8, lights off at 20:00 hr). Groups of 5 or 6 animals were sacrificed every hour during darkness.

Methods

Melatonin Assay

In all the following experiments the animals were killed at the indicated times by decapitation under

Melatonin was measured in the pineal gland by radioimmunoassay, using a rabbit antiserum (R19540,

Copyright r 1997 by Academic Press All rights of reproduction in any form reserved.

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Photoperiod and Melatonin Rhythm in the European Hamster

INRA, Nouzilly, France) and labeled [125I]-2-iodomelatonin. The assay has been previously validated for the European hamster (Pe´vet et al., 1989). The limit of sensitivity of the assay was 1 pg/tube, the minimum detection levels being 10 pg/pineal gland.

Data Analysis For data analysis, pineal samples that had undetectable concentrations of melatonin were assigned the value of the limit of sensitivity of the assay. To characterize the pattern of melatonin secretion in each experiment, nonlinear regression analysis was performed with TableCurve software (Jandel Scientific). Pineal melatonin profiles were fitted with the following equation (logistis peak): y 5 A 1 B · (1 1 10t2C )21 · (1 1 102(D2t))21 where y was the nth data point, t the time of the nth point, A the mean level during daytime, B the maximum of nocturnal peak (amplitude), C the inflection point at the onset of the peak, and D the inflection point at the decline of the peak (Fig. 1). In the following, C and D were used to characterize the timings respectively of the onset and of the decline of the peak. The duration of the melatonin peak was determined as the difference between C and D. The regression coefficients A, B, C, and D are given with their respective asymptotic SE estimates. When needed,

comparisons between regression coefficients have been made with unpaired Student’s test using these SE estimates; since these are overestimates, the significance of any difference was underestimated. All means were expressed 6 SE. A two-way analysis of variance was used to test the combined effects of temperature and time of the day (experiment 1, Fig. 1).

RESULTS Experiment 1 The effects of environmental temperature on the day and night pineal melatonin concentrations, in animals maintained in summer on a long photoperiod, are shown on Fig. 2. Daytime values were low and quite comparable in the three groups. The midnight concentrations still remained low and were not significantly different from the daytime values. There was a significant increase at the end of the dark period at 03:00 hr (1 hr before lights on) in the three groups (two-way ANOVA; probability for the effect of time P , 0.001). The data also show that the mean values at 03:00 hr are lower in animals maintained at 30° than in those maintained at either 10° or 20°. However, the probability of the time 3 temperature interaction just failed to reach significance (P , 0.06).

FIG. 1. The assymmetrical logistic curve which was fitted to melatonin profiles. (A) Baseline level (B) amplitude; (C and D) inflection points characterizing the position of the peak on the time scale.


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Experiment 2 Photoperiod greatly modified the amplitude, duration, and phase of the daily rhythm of melatonin synthesis (Fig. 3). As regards the amplitude (Figs. 3 and 4A), a small but significant peak was observed on LD 16/8 (54 6 21 pg/gland). The amplitude of the melatonin peak was markedly increased on LD 15/9 and reached a maximum for LD 14/10. For the other photoperiods, the amplitude of the peak was in the same range as that for LD 15/9, between 250 and 300 pg/gland. On photoperiods from LD 16/8 to LD 14/10, the onset occurred approximately 6 hr after the dark onset (Figs. 3 and 4B). On LD 12/12 and 10/14, the peak onset was advanced to nearly 4 hr after the dark onset. On the shortest photoperiod used, LD 8/16, the peak onset returned to 6 hr after the beginning of the night. The time of decline of the melatonin peak (Fig. 4B) increased gradually with the duration of the dark period. However, this increase was not regular and, for example, the decline occurred at the same time in LD 12/12 and 10/14, while the peak onsets differed. Moreover, the duration of the melatonin peak, determined as the difference between the onset and the decline,

FIG. 3. Nocturnal patterns of pineal melatonin concentrations under various artificial photoperiods. The dark bars represent the periods of darkness. Values are means 6 SE.

increased with the duration of the dark period. The data points could be fitted by a first-order regression line, with a correlation coefficient of 0.9535 (r 2 ) (Fig. 4C).

Experiment 3

FIG. 2. Effect of environmental temperature on the day and night pineal melatonin concentrations. The dark bar represents the period of darkness. Values are means 6 SE.


Figure 5 shows the patterns of change during summer of the night patterns of pineal melatonin concentration in animals maintained in natural outdoor conditions. On June 10th, close to the summer solstice (LD

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FIG. 4. (A) Changes in the amplitude of the night peak of pineal melatonin under decreasing photoperiods. Values are means 6 SE. (B) Changes in the onset and offset of pineal melatonin synthesis under decreasing photoperiods. Values are means 6 SE. (C) Relation between the duration of the night peak of pineal melatonin and decreasing photoperiods. (correlation coefficient, r 2 5 0.9535).

16/8), mean values remained low during the whole night except for a very short increase in melatonin concentration 1 hr before sunrise. Using one-way ANOVA, followed by Duncan’s multiple range test, melatonin concentrations at 04:00 were significantly different from those at other times of the day (P , 0.05). On August 3rd (LD 15/9), there was a significant night peak of pineal melatonin. The analysis revealed an amplitude of 245 6 30 pg/gland, the onset and the decline occurring, respectively, at 6.21 6 0.14 and 8.38 6 0.25 hr after the dark onset. The duration of the peak was 2.17 hr. The comparison with the profile obtained in artificial LD 15/9 did not show any significant difference for any component. On September 15th, close to the autumn equinox (LD12/ 12), there was an increase in both the duration and amplitude of the night peak of melatonin compared to that in August. The melatonin peak had an amplitude of 357 6 41 pg/gland, the onset and the decline occurred, respectively, 4.95 6 0.37 and 10.87 6 0.73 hr after the dark onset; the duration of the peak was 5.92 hr. Again, statistical analysis revealed no significant differences between the profiles obtained under natural conditions and those observed under an artificial photoperiod (LD 12/12). Comparing these three patterns, not only the duration but also the amplitude of the night peak of melatonin increased as day length decreased from June

to September. The profiles of melatonin rhythm did not significantly differ between natural and artificial conditions and in both cases an advance in the onset of melatonin synthesis was observed when the duration of the night or the dark period increased.

Experiment 4 In animals maintained on LD 16/8 in November, a clear melatonin peak was observed (Fig. 6). The onset and the decline of the peak occurred, respectively, 5.65 6 0.45 and 7.63 6 0.24 hr after the dark onset; the duration of the peak was 1.98 hr. According to the analysis of the melatonin profiles, these results were not significantly different from those obtained in June, at which time onset and decline occurred, respectively, 5.64 6 0.65 and 7.31 6 0.29 hr after the dark onset, the duration of the peak being 1.67 hr. Nevertheless, in November the amplitude of peak reached 217 6 62 pg/gland. This value was significantly higher than that observed in July (54 6 21 pg/gland) (P , 0.01).

DISCUSSION The present results show that photoperiod and environmental temperature are both involved in the


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regulation of the seasonal variations in the melatonin daily rhythms of the European hamster. Natural or experimental changes of photoperiod clearly affect the duration, the amplitude, as well as the phase relationships of the onset and the decline of melatonin synthesis with the light–dark or the dark– light transitions. As demonstrated by the correlation (Fig. 4C) between the duration of the dark period and the duration of elevated melatonin concentration (determined as the difference between the times of onset and decline of melatonin), the duration of the night peak of melatonin in the European hamster, as in most species studied to date, is directly dependent on the duration of the dark period (Vivien-Roels et al., 1988, 1992; Vivien-Roels, 1996; Pe´vet et al., 1991; Miche´ et al., 1991). It also appears that under experimentally controlled conditions, in addition to changes in duration, photoperiod induces changes in the amplitude of the night peak of melatonin. Indeed, under a decreasing photoperiod, from 16L/8D to 8L/16D, the amplitude increased considerably from 16L/8D to 14L/10D and then remained fairly constant under shorter photoperiods. There are now several studies that show that

FIG. 5. Nocturnal patterns of pineal melatonin concentrations under natural photoperiodic conditions. The dark bars represent the duration of the night, estimated from official sunset to official sunrise. Values are means 6 SE.


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FIG. 6. Nocturnal patterns of pineal melatonin concentrations under experimental long photoperiod at two times of the year, June and November. The dark bar represents the duration of darkness. Values are means 6 SE (June values are replotted from Fig. 3).

experimental changes in day length can affect the amplitude of the day–night melatonin rhythm. In the cat (Leyva et al., 1984), the Djungarian hamster (Illnerova et al., 1984; Lerchl et al., 1993; Miguez et al., 1996), or the marsh rice rat (Edmonds et al., 1995), for example, the amplitude of the night peak of melatonin is significantly lower under long than under short photoperiods. In other species such as the tammar wallaby (McConnell and Tyndale-Biscoe, 1985) the amplitude of the day–night peak of circulating melatonin is higher under long than under short photoperiod. In the domestic German landrace sow, a nocturnal surge in plasma melatonin concentrations was only observed in animals kept under a photoperiod of 12L/12D (McConnell and Ellendorf, 1987). When shifted to a longer or a shorter photoperiod the nighttime peak of melatonin secretion was abolished. This result was confirmed in the same species by Reiter (1987a, and Reiter et al., 1987), who also noted that NAT activity did not exhibit a nocturnal rise in long or short photoperiods. The present work shows that temperature, although less potent than photoperiod, also modulates the amplitude of the night melatonin peak, at least under


long photoperiodic conditions. It is well-known that in poı¨kilotherms the major external factor controlling the amplitude of the melatonin peak is environmental temperature (ref. in Vivien-Roels and Pe´vet, 1983; Vivien-Roels et al., 1988; Pe´vet et al., 1991; Vivien-Roels, 1996), but such an influence of temperature in mammals is incompletely documented. NAT and HIOMT activity have been reported to decrease in rats exposed to an ambient temperature of 33° for 24 hr (Nir et al., 1975; Nir and Hirschmann, 1978). In the suckling rat, Ulrich et al. (1973) noted that NAT activity was diminished when rats were exposed to either high (34°) or low (7°) temperature. Quay (1978) also reported photic and thermal influences on pineal activity and Stieglitz et al. (1991) showed that cold prevents the lightinduced inactivation of NAT in the Djungarian hamster. The present results demonstrate that, in the European hamster, photoperiod and temperature affect melatonin production, confirming previous observations on the seasonal variation in the midday and midnight pineal and circulating melatonin concentrations (Vivien-Roels et al., 1992). They might also explain the seasonal variation in the amplitude of the nocturnal peak of melatonin synthesis or NAT activity observed in many species kept under natural conditions, e.g., the sheep (Arendt, 1979; Sheikheldin et al., 1992), the horse (Guerin et al., 1995), the Djungarian hamster (Steinlechner et al., 1987, 1995), the tammar wallaby (McConnel, 1986), the European hamster (Pe´vet et al., 1989; Vivien-Roels et al., 1992), the deer (Paterson and Foldes, 1994), the goat (Kanematzu et al., 1989), and the mule (Cozzi et al., 1991). Depending on the species, the amplitude of the daily rhythm of melatonin secretion may be highest in summer and/or in autumn, e.g., in the tammar wallaby, the ram, or the horse (McConnell, 1986; Sheikheldin et al., 1992; Guerin et al., 1995), in winter and spring as in the golden or Djungarian hamster (Brainard et al., 1982; Steinlechner et al., 1995), or in autumn and winter such as in the European hamster (Vivien-Roels et al., 1992). Although there is considerable species variation it seems that in mammals as in nonmammalian vertebrates (Vivien-Roels, 1996), amplitude is an important characteristic of the daily pattern of melatonin. Its marked decrease may even explain the apparent disappearance of the daily melatonin rhythm observed

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under some natural or experimental photoperiodic conditions in the European hamster (Pe´vet et al., 1989; Vivien-Roels et al., 1992), the yellow-necked mouse (Apodemus flavicollis and Apodemus sylvaticus) (T. Ruf, personal communication), the Emperor penguin (Miche´ et al., 1991), the sheep (Thrun et al., 1995), and the German domestic landrace sow (McConnell and Ellendorf, 1987; Reiter et al., 1987). The differences observed in the present work in the amplitudes of the melatonin peak in European hamsters raised for 6 weeks under the same long photoperiod (LD 16/8) at two different times of the year, in June and November, also raise the question of the control of the seasonal variations in the amplitude of the melatonin rhythm. It is not possible, at the moment, to conclude if these differences in amplitude are the consequence of the previous photoperiod to which animals have been exposed (LP in June, SP in November) or to the presence of an endogenous circannual clock, as suspected in this species (Canguilhem et al., 1986; Masson-Pe´vet et al., 1995). Regarding the onset of pineal melatonin synthesis it appears that in the European hamster as in all rodent species studied so far there is a photoperiod-dependent delay between the time of the light–dark transition and the onset of melatonin synthesis. In the rat for example, NAT activity becomes significantly higher than the daytime value 2 hr after the beginning of the dark period in LD 16/8 but 3, 5, and 7 hr, respectively in LD 12/12, 8/16, and 6/18 (Illnerova, 1986; Illnerova and Vanecek, 1983, 1987). A similar observation, an increase in the delay of melatonin synthesis when darkness increases, has been reported in the Djungarian hamster (Hoffman et al., 1983; Illnerova et al., 1984). The European hamster is completely opposite. With respect to the light/dark transition, melatonin production starts 2 hr later under long photoperiod (LD 16/8, 15/9, 14/10) than under short photoperiods (LD 12/ 12, 10/14). This raises the question of the control of the onset of melatonin synthesis in the European hamster. Melatonin production (or NAT activity rhythm) is controlled via noradrenergic fibers originating from the superior cervical ganglia, by a circadian clock located in the suprachiasmatic nuclei (Klein and Moore, 1979; Klein et al., 1991). In the rat and the Djungarian hamster, it has been hypothetized that there might be a two-component pacemaker in the circadian clock con-


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trolling NAT and melatonin rhythms, the increased melatonin being controlled by an evening component coupled to dusk and its morning decline by a morning component coupled to dawn (Illnerova and Vanecek, 1982, 1987). The phase relationship between the two components and hence the period of elevated melatonin synthesis might thus be compressed under long days and decompressed under short days. Such decompression under short days would explain the progressive delay observed in the rat and the Djungarian hamster. In the European hamster the present results cannot be explained by such decompression of the clock, since the changes were observed in the opposite direction. It is difficult, at present, to explain these results, but it should be pointed out that they are not restricted to the European hamster. A similar observation has been made in another rodent species living in a tropical region, Arvicanthis niloticus (Vivien-Roels, unpublished data). This again stresses the complexity of the mechanisms involved in the regulation of the melatonin synthesis and the importance of comparative studies. With respect to the morning decline of melatonin synthesis in relation with the photoperiodic conditions, the European hamster also differs from the rat. In the latter, melatonin production declines spontaneously before the light onset even under a very long photoperiod (Illnerova and Vanecek, 1987). In contrast, in the European, Syrian, and Djungarian hamsters (Pitrosky et al., 1995; Lerchl et al., 1993), the morning decline in melatonin synthesis depends on the photoperiod. Under a long photoperiod the decline is induced by the onset of light, while under short photoperiods, the morning decline is endogenous and starts before lights go on. When comparing the sequence of onset, duration, and decline under various natural or experimental photoperiods in the European hamster, it appears that although the time of onset is not consistently delayed with decreasing photoperiod as it is in the rat (Illnerova and Vanecek, 1984), the duration of nocturnal melatonin production increases linearly. This suggests that there is a clear phase relationship between the onset and duration and that, at least under short photoperiods, the decline is directly dependent upon the onset of melatonin synthesis, rather than on the


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time of dawn or lights on. This might explain why under different photoperiods such as LD 12/12 and LD 10/14, the decline occurs exactly at the same time, unaffected by the longer dark period in LD 10/14 and raises the question of the possible presence of a regulation by a two-component pacemaker system coupled to dusk and dawn, as has been suggested in the rat (Illnerova, 1986). The present data suggest that in the European hamster, photoperiod is the main environmental factor implicated in the control of the seasonal variations of the daily pattern of melatonin synthesis. Photoperiodic changes result in wide changes not only in the duration but also in the amplitude, onset, and decline of the night peak of melatonin. Temperature, however, under long photoperiod has a clear effect which must also be considered. Indeed, the decrease in amplitude observed under high temperature conditions, together with the long photoperiod, might explain the disappearance of the rhythmic melatonin production observed in summer (long photoperiod, high temperature), although the circadian system is normally functioning at this time (Pe´vet et al., 1991). The results illustrate the complexity of the mechanisms involved in the regulation of the seasonal variations of the daily pattern of melatonin synthesis. The differences observed in the onset, decline, and amplitude of the melatonin peak cannot be explained only by a nocturnal increase in NE release from the sympathetic fibers innervating the pineal gland. They suggest that other neural regulatory mechanisms are also involved.

ACKNOWLEDGMENT The authors thank Dr. J. P. Ravault (INRA, Nouzilly, France) for kindly providing the melatonin antiserum.

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