Influence of pinealectomy and pineal stalk deflection on circadian gastrointestinal tract melatonin rhythms in zebra finches (Taeniopygia guttata).

The authors examined levels of melatonin in the plasma and various tissues in intact, pinealectomized, and pineal stalk-deflected zebra finches kept under 12:12 LD to determine if the melatonin found in the gastrointestinal tract is secreted in a circadian manner. In intact and pineal stalk-deflected birds, there is a clear day-night rhythm in melatonin content of the plasma, pineal gland, eyes, proventriculus, crop, duodenum, jejunum/ileum, colon, heart, and liver. In contrast, pinealectomy abolished the day-night rhythm. These results indicate that most of the melatonin present in the gastrointestinal tract of zebra finches is of pineal origin. However, some melatonin remained. This suggests that this melatonin may be locally synthesized and has paracrine and/or autocrine functions. Nonetheless, the results do not lend support to the contention that this putative melatonin secretion by the gastrointestinal tract is circadian.

Exogenous melatonin reduces the resynchronization time after phase shifts of a nonphotic zeitgeber in the house sparrow (Passer domesticus).

Continuous melatonin administration via silastic implants accelerates the resynchronization of the circadian locomotor activity rhythm in house sparrows (Passer domesticus) after exposure to phase shifts of a weak light-dark cycle. Constant melatonin might induce this effect either by increasing the sensitivity of the visual system to a light zeitgeber or by reducing the degree of self-sustainment of the circadian pacemaker. To distinguish between these two possible mechanisms, two groups of house sparrows, one carrying melatonin implants and the other empty implants, were kept in constant dim light and subjected to advance and delay shifts of a 12-h feeding phase. The resynchronization times of their circadian feeding rhythm following the phase shifts were significantly shorter when the birds carried melatonin implants than when they carried empty implants. In a second experiment, melatonin-implanted and control birds were released into food ad libitum conditions 2 days after either a delay or an advance phase shift. The number of hours by which the activity rhythms had been shifted on the second day in food ad libitum conditions was assessed. Melatonin-implanted house sparrows had significantly larger phase shifts in their circadian feeding rhythm than control birds. This is in accordance with the first experiment since a larger phase shift at a given time reflects accelerated resynchronization. Additionally, the second experiment also excludes any possible masking effects of the nonphotic zeitgeber. In conclusion, constant melatonin accelerates resynchronization even after phase shifts of a nonphotic zeitgeber, indicating that constant high levels of melatonin can reduce the degree of self-sustainment of the circadian pacemaker independent of any effects on the photoreceptive system.

Seasonal and daily variations in plasma melatonin in the high-arctic Svalbard ptarmigan (Lagopus mutus hyperboreus).

This study presents the daily rhythm of melatonin secretion throughout one year in a bird from the northern hemisphere, the Svalbard ptarmigan (Lagopus mutus hyperboreus), which lives naturally at 76-80 degrees N. Eight Svalbard ptarmigan were caged outdoors at 70 degrees N and blood sampled throughout one day each month for 13 months. At this latitude, daylight is continuous between May and August, but there is a short period of civil twilight around noon from late November to mid January. There was no daily rhythm in plasma melatonin in May-July. Plasma melatonin levels varied significantly throughout the day in all other months of the year, with the nighttime increase reflecting the duration of darkness. The highest mean plasma concentration occurred at midnight in March (110.1 +/- 16.5 pg/ml) and represented the annual peak in estimated daily production. Around the winter solstice, melatonin levels were significantly reduced at noon and elevated during the nearly 18 h of consecutive darkness, and the estimated mean daily production of melatonin was significantly reduced. Thus, at the times of the year characterized by light-dark cycles, melatonin may convey information concerning the length of the day and, therefore, progression of season. The nearly undetectable low melatonin secretion in summer and the reduced amplitude and production in midwinter indicate a flexible circadian system that may reflect an important adaptation to life in the Arctic.

Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris).

Tropical birds usually lay smaller clutches and are less likely to initiate a second brood than their temperate-zone relatives. This reduction in annual fecundity is generally explained as an adaptation either to higher rates of nest predation or to a more limited food supply concurrent with higher adult survival in the tropics. However, the physiological parameters associated with lower annual fecundity in tropical birds have not been well investigated. We compared the annual fecundity, behaviour and a number of physiological parameters of stonechat parents feeding fledged juveniles in territories with and without fiscal shrikes, a predator on adult and fledged birds. Stonechat pairs in territories with shrikes were less likely to initiate a second brood and delayed successive broods compared to pairs in territories without shrikes. After fledging of their young, males showed a greater propensity than females to initiate distraction calls after a human intrusion into their territory and, therefore, invested more in the defence of their young. In territories with shrikes stonechat males had higher initial plasma corticosterone levels and lower body conditions than males in territories without shrikes, suggesting that they were chronically stressed. In contrast, the females from both types of territory had low initial plasma corticosterone levels. We conclude that shrike presence might account for the delay in initiation of a second brood and the reduction in the tendency to initiate a second brood. Whether these effects are mediated by the elevated levels of corticosterone remains to be demonstrated.

Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.

Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.

Circadian rhythms of melatonin in European starlings exposed to different lighting conditions: relationship with locomotor and feeding rhythms.

In passerine birds, the periodic secretion of melatonin by the pineal organ represents an important component of the pacemaker that controls overt circadian functions. The daily phase of low melatonin secretion generally coincides with the phase of intense activity, but the precise relationship between the melatonin and the behavioral rhythms has not been studied. Therefore, we investigated in European starlings (Sturnus vulgaris) (1) the temporal relationship between the circadian plasma melatonin rhythm and the rhythms in locomotor activity and feeding; (2) the persistence of the melatonin rhythm in constant conditions; and (3) the effects of light intensity on synchronized and free-running melatonin and behavioral rhythms. There was a marked rhythm in plasma melatonin with high levels at night and/or the inactive phase of the behavioral cycles in almost all birds. Like the behavioral rhythms, the melatonin rhythm persisted for at least 50 days in constant dim light. In the synchronized state, higher day-time light intensity resulted in more tightly synchronized rhythms and a delayed melatonin peak. While all three rhythms usually assumed a rather constant phase relationship to each other, in one bird the two behavioral rhythms dissociated from each other. In this case, the melatonin rhythm retained the appropriate phase relationship with the feeding rhythm.

Development of post-hatching melatonin rhythm in zebra finches (Poephila guttata).

We examined levels of melatonin in the pineal, eyes and plasma over a 24 h period during development in the altricial zebra finch. Beginning as early as 2 days after hatching there was a distinct 24 h rhythm in melatonin in the pineal and plasma. Beginning at day seven after hatching there was also a 24 h rhythm present in the eyes. In the pineal and eyes the amplitude of the 24 h rhythm increased with age. In contrast, the amplitude of the plasma melatonin rhythm at 2 days was already within the range of adults and did not increase with age. These results confirm and expand earlier findings in the European starling and parallel those from precocial birds indicating that the circadian system is already competent at or shortly after hatching even in atricial birds.

Melatonin is rhythmic in newborn seals exposed to continuous light.

We have investigated the effect of continuous light and darkness on plasma levels of melatonin in relation to the extremely large and active pineal gland typically found in newborn seals. Plasma levels of melatonin in captive newborn harp (Phoca groenlandica) and hooded seals (Cystophora cristata) were generally extremely high, with peak concentrations ranging from 0.8 ng/ml to 62.3 ng/ml. Moreover, plasma melatonin showed a similar, pronounced rhythmicity, both outdoors under natural light conditions (hooded seal only) and indoors under either 30 h of continuous light (490 lux) or 30 h of darkness (0 lux). In all animals, the melatonin rhythm was closely associated with the outdoor light-dark cycle. We suggest that the melatonin rhythmicity in newborn seals is mainly under circadian control and that it originates by maternal influence in the foetus. Daytime plasma concentrations of melatonin were also measured in foetal hooded seals and their mothers. The foetal melatonin level was similar to daytime levels in newborns and was about five times higher than in their mothers, which indicates a significant flow of foetal melatonin to the mother. We speculate that the large pineal gland and high melatonin levels in the newborn seals are temporary consequences of a foetal strategy to affect the maternal blood supply during diving.

Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin.

Neuroplasticity in the vocal control system of songbirds is strongly influenced by seasonal fluctuations in circulating testosterone. These seasonally plastic telencephalic structures are implicated in the learning and production of song in songbirds. The role of the indoleamine melatonin in seasonal adaptations in birds has remained unclear. In this experiment, European starlings were castrated to remove the neuromodulating activity of gonadal steroids and were exposed to different photoperiods to induce reproductive states characteristic of different seasonal conditions. Long days increased the volume of the song-control nucleus high vocal center compared with its volume on short days. Exogenous melatonin attenuated the long-day-induced volumetric increase in high vocal center and also decreased the volume of another song-control nucleus, area X. This effect was observed regardless of reproductive state. To our knowledge, this is the first direct evidence of a role for melatonin in functional plasticity within the central nervous system of vertebrates.

Seasonal variations of in vivo and in vitro melatonin production in a passeriform bird, the house sparrow (Passer domesticus).

Melatonin, released from the pineal gland, is an important signal within the circadian pacemaking system of passeriform birds. Until now, seasonal variations in melatonin production have only been examined in a few avian species and the role of melatonin in the regulation of annual rhythms in birds is unclear. We investigated plasma melatonin in a group of house sparrows kept in an outside aviary in spring (March/April), summer (May/June), autumn (September/October), and winter (December/January). The durations of elevated melatonin values mirrored the seasonal changes in night length to a certain degree, the melatonin signal being longest in winter and shortest in summer. Additionally, plasma melatonin peak amplitudes differed significantly among seasons, with highest values in spring and summer and lowest values in winter. Cultured explanted pineal glands obtained from animals in winter and summer showed patterns of in vitro melatonin release comparable to in vivo circulating melatonin with different durations of elevated melatonin and peak amplitude values. These data indicate that the circadian pacemaking system of the house sparrow changes properties seasonally, either as a result of endogenous mechanisms or in response to environmental conditions. These properties are maintained in the pineal gland even after isolation from the animal.