Biological rhythms in Arctic vertebrates

Many biological processes show regular cyclical fluctuations that persist throughout an organism's life; these range from the transcription of DNA to patterns of behaviour. Persistent, cyclical phenomena of this kind are a fundamental feature of all organisms. They are governed primarily by endogenous rhythms generated by a 'biological clock' situated in the btain. Normally, however, the expression of the clock is modulated to a greater or lesser extent by environmental cues. This paper reviews the physiological control of the temporal organisation of cycles in vertebrates and, in particular, explores their regulation in arctic species like reindeer (Rangifer tarandus L.). We emphasise how exposure to the photoperiodic conditions that characterise polar regions places special demands on timing mechanisms and how arctic species, therefore, are of particular interest for the study of biological rhythms. Thus far, behavioural and physiological studies of these species show that arctic reindeer (and ptarmigan) appear to be truly opportunistic in summer and wintet, seemingly without any active biological clock and that they are, instead, driven directly by photoperiod. This situation, if confirmed, would be unique among vertebrates.


Introduction
Many biological processes show regular cyclical fluctuations that persist throughout an organism's life; these range from the transcription of DNA to patterns of behaviour.Persistent, cyclical phenomena of this kind are a fundamental feature of all organisms.They are governed primarily by endogenous rhythms generated by a 'biological clock' situated in the brain.Normally, however, the expression of the clock is modulated to a greater or lesser extent by environmental cues.This paper reviews the physiological control of the temporal organisation of cycles in vertebrates and, in particular, explores their regulation in arctic species, like reindeer (Rangifer tarandus L.), which are exposed to the photoperiodic conditions that characterise polar regions.

The basic problem
In many species, daily and annual cycles in physiological and behavioural parameters are closely corre-lated with day length, usually referred to as 'photoperiod' (Table 1).Organisms can extract two kinds of information by monitoring the duration of the daily photoperiod: the daily light/dark cycle provides them with a 24 hour clock and changes in daylength provide them with a calendar indicating the changing of the seasons.In these two ways photoperiod provides an absolutely secure, predictable signal for keeping track of time in what are otherwise often unpredictable environments.Plants and animals living at 30-60°N lat. in the northern temperate zone experience a strongly rhythmic and dynamic photoperiodic environment with clear daily light/dark cycles and pronounced seasonal changes in daylength (Fig. 1).Not surprisingly, therefore, photoperiod plays a major role in the regulation of temporal organisation in temperate species.Arctic species, such as reindeer and muskox (Ovibos moschatus), by contrast, live in regions where photoperiodic information is much reduced or even absent for considerable periods of the year.These animals are exposed to continuous daylight, the Synchronisation of the phase of the biological clock with the correct phase of the environment.Entrainment ensures the proper phase-relationships between particular body rhythms and the appropriate rhythmic changes in the environment.
Biological rhythm expressed under constant conditions.
A cycle with a frequency >>24 h., i.e. with less than (infra-) one cycle a day (diem).

Duration of night and day.
Endocrine gland in the brain.Innervated by sympathetic nerves from the SCN.Produces the hormone melatonin.
Period of continuous light in summer when the sun is continuously above the horizon.
Period of continuous darkness in winter when the sun is continuously below the horizon.
Suprachiasmatic nucleus.Structure in the hypothalamus where the mammalian biological clock is situated.
Independence of the frequency of a cycle from ambient temperature.
Time cue which signals the setting or resetting of the biological clock to the correct phase with respect to the time of the day or of the year.Light is the most important, but not the only, Zeitgeber.
'polar day', in summer and continuous darkness, the 'polar night', in winter.Nevertheless, they display pronounced, highly predictable annual cycles of metabolism, growth and behaviour.This simple observation suggests that the regulation of cyclical phenomena may be different in Arctic compared to temperate species.
The role of self-sustained, clock-driven, endogenous rhythms in the regulation of annual cycles of growth and behaviour is well documented in temperate ungulates such as red deer (Cervus elaphus: Loudon & Jabbour, 1994), white-tailed deer (Odocoileus virginianus: Brown et al., 1978) and sheep (Ovis aries: Lincoln, 1992; 1998).However, there is no convincing evidence for the role of a biological clock in the control of the corresponding cycles in reindeer and muskoxen.One way to identify the presence of an endogenous rhythm is to demonstrate that a cycle -the daily cycle of the production 100 of melatonin or the annual cycle of coat growth, for instance -persists while the animals are maintained under constant daylight conditions.However, this has not been investigated for arctic ungulates.
In a sense, of course, the necessary experiments are performed twice a year every year, for these are exactly the conditions to which animals living in their natural environment are exposed in mid-winter and mid-summer.Thus, the clear daily rhythms of behaviour which Svalbard reindeer (R.  (Akerstedt, 1979;Orth et al, 1979).Infradian rhythms include arousal during hibernation (e.g.ground squirrels Spermophilus lateralis: Ruby et al., 1996), menstruation, the annual cycle of growth and fattening in northern cervids (Leader-Williams & Ricketts, 1982; Suttie et al, 1983;Tyler, 1987;1995;Lincoln & Baker, 1995;Suttie & Webster, Hewison et al, 1996), the antler cycle in reindeer (Lincoln & Tyler, 1994), the annual moult of hair and feathers (Meijer, 1989;Stokkan & Sharp, 1990), breeding and migration (e.g.Lundberg & Eriksson, 1984).All these cyclical fluctuations occur regularly and spontaneously.They are not prompted by exogenous environmental cues but are triggered, instead, by endogenous signals that arise independent of, but may become modified by, the animals' environment.
An important test of the endogenous basis for an overt rhythm is the persistence of cyclicity even when the environment is held constant.To identify the endogenous basis of a rhythm one should, in addition, be able to demonstrate (i) that its phase can be altered by the manipulation of light/dark signals (Aschoff, 1964a;1999) and (ii) that it's expression is temperature compensated (Table 1).Golden hamsters' (Masocricetus auratus) daily cycle of wheel-running and the sleep/wake pattern of humans, for example, persist when the experimental subjects live in constant darkness (Jorgens, 1967;Aschoff, 1985).Had these cycles of activity been driven directly by the light/dark cycle, they would have been abolished immediately following the onset of constant light (or dark) conditions.
While the functional role of biological clocks has been demonstrated in a wide range of organisms, there is little direct experimental evidence of the adaptive significance of the circadian organisation which the clocks regulate.Nevertheless, it is generally accepted that organisms benefit from the temporal organisation of physiological functions and behaviour, chiefly because it enables them to anticipate daily and seasonal changes in their environment (Aschoff, 1964b).Thus, in plants, protein synthesis and the orientation of leaves anticipate the onset of daylight as well as the movement of the sun across the sky (Stayton et al, 1989;Levy & Moore, 1993).Honey bees (Apis mellifera) have a sense of time which allows them to anticipate the peak of the daily production of floral nectar and even find their way back to previously detected food stores by means of time-compensated sun-compass orientation (Aschoff, 1986;Frish & Aschoff, 1987;Moore et al, 1989).The immune function of deer mice (Peromyscus mankulatus) is enhanced (Demas & Nelson, 1998), reindeer fatten and grow a thick coat (Suttie & Webster, 1995) and Arctic waders migrate south all in advance of the onset of winter.Accurate timing of estrus and mating in northern species of deer ensures that the burden of lactation many months later coincides with the period when the females have access to abundant high quality forage.When aberrations in timing result in conceptions outside the normal breeding season, the unusually early-born or late-born calves suffer heavy mortality (Clutton- Brock et al, 1982).

The biological clock(s)
In mammals, the clock which generates circadian rhythmicity is situated in a region of the hypothalamus called the suprachiasmatic nucleus (SCN).The SCN consists of groups of neurons whose activity oscillates spontaneously with a frequency close to 102 24 hours.The oscillating frequency of the SCN as a whole is the mean of the activity of the individual cells.Neither the way in which the activity of the different cells is integrated, nor the way in which the net circadian rhythmicity of the SCN is translated into the regulation of the body's rhythmic functions is known, but the pineal hormone melatonin evidently plays an important role in this.
While the SCN plays a central role in generating endogenous circadian rhythms and, for this reason, is often referred to as the biological clock, it is not unique: there is a variety of oscillators in mammals which, singly or in combination, are involved in driving different behavioural and physiological rhythms.There are also different classes of oscillators, even within a single cell (Hoffmans- Hohn et al., 1984).Some are normally entrained by the light/dark cycle while others are entrained by other stimuli, such as the cyclical presentation of food.One such is the oscillator which regulates feeding activity in rodents (Boulos & Terman, 1980) Heintzen et al, 1997;Turek, 1998;Weaver, 1998).The discrepancy is small but significant.To the extent that the role of the SCN is to synchronise the animal to its environment, the clock must be reset from time to time.The resetting of the phase of the clock is called 'entrainment' (Table 1) and the environmental cues which serve to entrain it are called Zeitgebers' (Table 1).The best known Zeitgeber is the daily light/dark cycle which, at any given latitude, varies in an entirely predictable manner throughout the year.

Adjusting the clock
Diurnal mammals seem to entrain to the daily light/dark cycle through dynamic adjustments in SCN function which result in alteration of the phase and the frequency of the clock (Pittendrigh, 1981;Beersma et al., 1999).The phase of the clock may be advanced or delayed relative to the real (solar) time of day and its frequency may, likewise, be accelerated or decelerated.Adjustment of the phase of the clock appears to be a rapid response, while alteration of the clock's frequency seems to occur continually while the animal is awake (Beersma et al, 1999).
The sensitivity of the clock to the different kinds of temporal information to which it can become entrained varies throughout the day and is described in so-called 'phase response curves' (e.g.Pittendrigh, 1981).Sensitivity to photoperiodic information is characteristically high at the beginning and the end of the daily period of activity and low, or even absent, during the middle.These responses are species specific: for example, golden hamstets are highly responsive to photic information while white-footed mice (Peromyscus leucopus) are much less responsive (Pittendrigh & Daan, 1976).The functional significance of these differences is unclear.It may be that low sensitivity to environmental zeitgebers enhances opportunistic behaviour.This might be highly beneficial, for example, in animals moving from one rhythmic environment into another.Birds appear to reduce their zeitgeber sensitivity while migrating across many degrees of longitude (Gwinner et al, 1997); the pineal gland of lampreys (Petromyzon marinus) altogether ceases to synthesise melatonin while the animals are switching hosts (Menaker & Tosini, 1996).Whatever the adaptive significance of these differences in zeitgeber sensitivity, they are reflected in the amplitude of the daily cycle in the plasma 104 concentration of the hormone melatonin (Hau & Gwinner, 1997).Melatonin is a hormone of darkness: it is secreted at night and its secretion is suppressed by light during the day.This can be misleading, because the secretion of melatonin is a response to the endogenous rhythm of the SCN, not to darkness itself.In most mammals, the rhythmic secretion of melatonin persists during exposure to several days of constant darkness (Scott et al., 1995).Light does, however, play a role in the regulation of the secretion of melatonin by inhibiting the SCN from stimulating the pineal production of the hormone (Reiter, 1993).

The role of melatonin in the regulation of biological rhythms has been well demonstrated in ungulates, particularly with regard to the timing of reproduction in seasonal breeders. Photoperiod has clear inductive effects on reproduction in both red deet and sika deer (Cervus nippori
).An artificial change from long to short days induced premature reactivation of the reproductive axis owing to its signalling the early onset of autumn (Goss, 1969).Treatment with melatonin in spring and summer gives the same signal and the same result.Artifically increasing the duration of exposure to the hormone induces autumnal (short-day) responses such as the premature reactivation of testicular acrivity and the early onset of ovulatory cycles in red deer (e.g.Lincoln et al, 1984;Webster & Barrell, 1985;Adam et al., 1986).
There is one important caveat.The alteration of the timing of reproduction by the manipulation of photoperiod or of circulating levels of melatonin or in response to dietary and social factors (Martin, 1984) demonstrates ways in which environmental cues can modulate the overt expression of an underlying, endogenous rhythm.None of these observations, however, preclude the central role of the clock in establishing the basic seasonal (or daily) rhythm.Clear evidence for this is provided by the persistence of physiological cycles in animals maintained under constant photoperiod, such as the seasonal rise in blood levels of luteinizing hormone in ovariectomised ewes kept on short days for 2.5 years (Branson, 1989: 118), or the persistence of the antler, pelage and other cycles in deer (Goss, 1969;1974;Loudon & Brinklow, 1992)  Gardens (51°30'N lat.: Lincoln, 1985).The expression of the endogenous rhythms which regulated the breeding season in these deer persisted and was not modified by the characteristics of the photoperiod to which they were latterly exposed.

Rhythms in the Arctic
The

Activity rhythms in arctic residents
High arctic residents respond quite differently to continuous light conditions.Two sub-species have been studied in considerable detail while living under natural light conditions: Svalbard ptarmigan, the only herbivorous bird permanently resident on the high arctic archipelago of Svalbard, and Svalbard reindeer.Both these sub-species behave similarly in response to changes in their photoperiodic environment.As expected, they display daily rhythms of activity while exposed to the daily light/dark cycles of late summer (September-October) and late winter (February-March).In midsummer and mid-winter, by contrast, the animals become intermittently active around the clock (Stokkan et al, 1986;Reierth & Stokkan, 1998;van Oort etal, 1998;1999a In contrast to this, most, though not all, individual arctic ground squirrels (Spermophilus undulatus) and brown lemmings (Lemmus trimucronatus) maintained rhythmic cycles of activity when exposed to natural summer light conditions at 70°N (Swade & Pittendrigh, 1967).The behaviour of these individuals, therefore, was governed endogenously as in snow buntings and humans (Kriill, 1976;Johnsson et al., 1979).It is evident that considerable variation exists both within and between species in the ways in which the biological clock responds to the special photic conditions which characterise high latitudes.

Rhythms in arctic ungulates
Many cyclic phenomena have been described in Arctic ungulates.These include seasonal variation in activity rhythms (muskoxen: Jingfors, 1982; Oakes et al., 1992 Ringberg et al, 1978;Ryg & Jacobsen, 1982;Nilssen et al, 1985;Suttie etal, 1991;Bubenik etal, 1997;1998).Notwithstanding the variety of phenomena which have been described, little is known about the regulation of these cycles.Recent work on two sub-species of reindeer, however, provides some intriguing clues.Like in Svalbard reindeer (above), the marked daily rhythms of activity which mainland reindeer (R. t. tarandus) living at 70°N lat.show in late winter also break down under the continuous light conditions of summer.Their daily bouts of activity become evenly distributed across the 24 hour day such that they are just as likely to be active at midnight as at noon (van Oort et al, 1998;1999b).Like Svalbard reindeer, therefore, mainland reindeer seem to have only weak circadian mechanisms in summer.

Interestingly, these two sub-species of reindeer
RangiEer, 20 (2-3), 2000 seem to respond differently to the continuous darkness of winter in their respective natural evironments.While Svalbard reindeer become arrhythmic during the polar night, showing activity around the clock as in summer, mainland reindeer living freely at 70°N lat.remain synchronised with the 24 hour day.Their main bout of activity occurs in the middle of the day and the timing of the onset of activity early in the morning remains highly predictable throughout the winter (van Oort et al, 1998;1999b).In both situations where these studies were carried out (at 70° and 78°N lat.) the sun remains permanently below the horizon in the middle of winter: mainland reindeer, nevertheless, were capable of responding to the weak diurnal fluctuation in the level of twilight that occurs during December and January at 70°N lat.These results can be intetpreted in one of two ways.Either mainland reindeer are entrained by the weak photic information which is available in winter, or their clock function is suppressed and activity is regulated, instead, directly by changes in light intensity.The key difference between these alternatives may be the level of SCN activity and the functional significance of the clock in winter.This can be explored by studying the pattern of secretion of melatonin which lies closer to the clock than the rhythm of activity and which might, therefore, mote accurately reflect clock function.

Melatonin rhythms in arctic ungulates
Only three groups have investigated the roles of photoperiod and melatonin in the control of endogenous mechanisms in arctic ungulates (muskoxen: Tedesco et al, 1992;reindeer: Eloranta et al, 1992;1995;Stokkan et al, 1994).A null hypothesis in all these studies is that clock function is maintained throughout the year and, reflecting this, the citcadian rhythm of the secretion of melatonin persists throughout the polar night and the polar day.Were this the case, the observed breakdown of the daily rhythms of locomotor activity in mid-summer and mid-winter in reindeer would be attributable to an uncoupling of the influence of the melatonin cycle from the regulation of activity.If the null hypothesis is rejected, i.e. if the circadian rhythm of the sectetion of melatonin is lost in midsummer and mid-winter, two alternative explanations for the arrhythmicity of activity arise.Either clock function must be shut down or it persists while the link between the SCN and the pineal is somehow interrupted.
The daily cycle of the secretion of melatonin has been studied in reindeer living under natural light conditions at 70°N lat.Both Eloranta et al. (1992) and Stokkan et al. (1994) demonstrated the presence of robust daily rhythms in the plasma concentration of melatonin in spring and autumn while in summer the cycle disappeared altogether and the daily production of melatonin fell to an annual minimum.The results from mid-winter trials diverged slightly.Eloranta et al. (1992) apparently detected a weak daytime reduction in the plasma concentration of melatonin.Stokkan et al. (1994), however, were unable to replicate this result and detected no daily rhythm in the secretion of melatonin in reindeer in December.Taken together, these studies suggest that the breakdown of the daily rhythmicity of activity in reindeer in summer is associated with the suppression of the daily rhythm of the secretion of melatonin, while leaving aside the question of the level of clock function at this time.Eloranta et al. (1995) Fig.1 , pigeons (Columba livia:Phillips et al., 1993) and house sparrows(Passer domesticus: Hau & Gwinner,  1992).The existence of oscillators of this kind is easily overlooked because in nature the availability of food is often closely linked to the light/dark cycle (e.g. the abundance of insects eaten by insectivorous birds).Thus, while the activity of the birds, for example, is tightly correlated to light conditions, the relationship may be only indirect.The role of multiple or compound clocks in regulation of the temporal organisation of behaviour has been demonstrated by the experimental separation of rhythms that were apparently inextricably linked and by recording the subsequent independent persistence of each(Mrosovsky & Hallonquist, 1986).The mammalian SCN, therefore, is better considered not as the clock but as the master dock, the chief among many.This view represents a widely accept

Fig. 2 .
Fig. 2. The figure shows the revolution of the Earth around its axis and the consequential occurence of night and day.Seasons are a result of the tilting of the Earth's axis which causes different parts of the Earth, in turn, to face predominantly towards or away from the sun.The seasons are indicated for the northern hemisphere.The arrows show how sunlight is absent north of the Arctic circle in winter, while there is continuous daylight there in summer.
The occurrence of day and night is due to the rotation of the planet around its axis as a result of which every point of the surface of the Earth moves alternatively into and out of direct view of the sun.The Earth completes one rotation every 24 hours.In addition, it revolves around the sun, completing Rangifer, 20 (2-3), 2000 one cycle approximately every 365 days.The occurrence of seasons, which so influence the life history of temperate and polar species, is a consequence of the fact that the axis of the Earth is tilted at 23.5° relative to the plane of its orbit.The poles, therefore, alternately face mainly towards or mainly away from the sun (Fig.2).In the northern hemisphere, we enjoy the long days of summer when the North Pole is tilted towards the sun while in winter, when the situation is reversed, the days are short.Seasonal variation in daylength increases with increasing latitude.At high latitudes, the daily light/dark cycle disappears both in mid-summer when the sun remains continually above the horizon (the 'polar day') and in mid-winter, when the sun remains continually below the horizon (the 'polar night').At Tromsø, 70°N lat., the polar day lasts 69 days and the polar night lasts 51 days (Fig.1).Information on daylength at different latitudes is available at http:llaa.usno.navy, millAAidata!.Receiving and conveying photoperiodic information to the rest of the bodyNo animal can be entrained by the light/dark cycle unless it posseses a superficial photoreceptor (although seeCampbell & Murphy, 1998;Yamazaki et al, 1999).In mammals, photoperiodic information is transmitted to the SCN via neural relays from photoreceptors in the retina which, independent of the visual pathway, are concerned only with entrainment of the circadian clock(Miyamoto & Sancar, 1998).An animal can, therefore, be visually blind but still receptive to photoperiodic information.The retinohypothalamic tract -a projection with no visual function -is believed to be the major route along which photic information is fed into the circadian system although other inputs from the primary and accessory optic tracts also exist(Hofmann, 1981;Menaker & Binkley, 1981).
The information represented by the output of the SCN, which integrates an endogenous component with photoperiodic modulation, is presumably transmitted to the rest of the body by the daily fluctuation in the plasma concentration of melatonin.This hormone appears to be a key intermediate between the biological clock -the SCN -and rhythms of behaviour and physiological function.Melatonin is secreted by the pineal gland which lies between the cerebral hemispheres above the third ventricle of the brain where it receives sympathetic innervation from the SCN (Lincoln, 1998; Fig. 3).Changes in the plasma concentration of melatonin convey two kinds of information.The daily fluctuation in concentration makes distinction between day (low melatonin) and night (high melatonin) while, in species living in the temperate zone, the duration of the night-time peak of melatonin indicates season, varying from summer (short duration) to winter (long duration).Thus, the duration of the nighttime peak of melatonin shortens as the days grow longer in spring, reaches a minimum in summer, lengthens as the days grow shorter in autumn and reaches a maximum in winter.

Fig. 3 .
Fig. 3. Schematic plan of the brain illustrating the circadian and circannual axis after a model for a tempetate zone long-day breeding mammal.The dotted line shows the pathway along which photoperiodic information is transmitted to the pineal gland.Light acts both to entrain the phase of the daily endogenous rhythm of the SCN and to suppress melatonin secretion in the pineal gland.The two bold arrows show the pathways along which photoperiodic information, translated into a melatonin rhythm, is believed to influence daily and annual rhythms of physiological function and behaviour.The duration of melatonin secretion acts, for example, via the pituitary gland to modulate the pulsatile sectetion of GnRH, thus regulating the activity of the reproductive axis.Daily and annual rhythms are also modulated by non-photic environmental input.(SCN = suprachiasmatic nucleus, SCG = supracervical ganglion, LH = Luteinising hormone, GnRH = Gonadotropin releasing hormone).
life-history of arctic animals exemplifies biological timing in an extreme form.Accurate timing of breeding, rearing young, moulting etc. is particularly important in the Arctic where the ambient temperature may rise above freezing for just a few weeks in summer.Consequently, the degree of synchrony of these and other life-history events within populations generally increases markedly with increasing latitude (e.g.Lincoln, 1998).How is this timing achieved at latitudes characterised by the absence of any marked light/dark rhythm in midsummer and mid-winter which might regulate clock function?We can explore this question using two groups of animals: summer visitors and arctic residents.Visitors, such as migratory birds, are exposed to daily light/dark cycles throughout the year except in mid-summer when they breed and rear their young before departing south.Residents, on the other hand, are exposed to a daily light/dark cycle in late winter and late summer but live under continuous light conditions for the remainder of the year.Activity rhythms in summer visitorsSnow buntings (Plectrophenax nivalis) visit Svalbard (74-8TN lat.) in summer to breed.Their daily rhythms of locomotor activity persist throughout the summer and appear to be entrained by the solar cycle(Kriill, 1976).The birds are evidently able to extract photoperiodic information from the continuous daylight conditions of the arctic summer.Similar observations have been made in a variety of birds and mammals exposed to summer light conditions near the Arctic circle (66°N lat.), including species which do not normally penettate so far north (Daan & Aschoff, 1975).All species which perform in this manner must have a strong sensitivity to the zeitgeber, thereby being able to extract photoperiodic information even under the continuous daylight conditions of the polar day.The exact nature of the cue is unknown; it might be the changing azimuth of the sun or the changes in the spectral composition of light which occur during the course of the 24 hour day (Kriill, 1976).106 Humans, by contrast, behave quite differently.Unlike snow buntings, the summer visitors to Svalbard studied by Johnsson et al. (1979) displayed free-running rhythms of body temperature and sleep-wake cycles which soon fell out of phase with the solar, 24 hour day.Humans, therefore, appear to be less sensitive to the photic zeitgeber than snow buntings and are unable to extract photoperiodic information during the continuous daylight conditions of the high arctic summer.Human subjects at 70°N lat.(Tromsø) have been shown to synchronise their melatonin rhythm to the 24 hour day both in summer and winter (Stokkan & Reiter, 1994) but the resultant rhythmicity of the sleep-wake cycle is not strong and sleep disturbances are frequently reported at this location (Lindgjaerde et al, 1985).Clearly, sensitivity to continuous light conditions is species specific.
; b; van Oort, unpubl.data).These results indicate that Svalbard reindeer and Svalbard ptarmigan have weak circadian mechanisms: either weak endogenous pacemakers or low sensitivity to the subtle changes in photic conditions which entrain snow buntings in summer.Consequently, these animals are able to feed opportunistically around the clock during the polar night and the polar day as conditions permit, unconstrained by any endogenous cont ol of the temporal pattern of their daily activity.Similar results have been observed in tundra voles (Microtus oeconomus) and red-backed voles (Clethrionomys rutilus) at 70°N (Swade & Pittendrigh, 1967).In every case, the animals failed to show any free-running or entrained rhythms of activity under continuous light conditions, indicating either loss of the normal coupling between clock function and behaviour or between the rhythm generating cells within the SCN or even a 'switching-off' of the clock.
took a first step towards investigating clock function with an important experiment in which reindeer were put into a dark room in the middle of the day in mid-summer.The animals, which had been exposed to continuous, natural daylight for several weeks, responded with an immediate rise in the plasma concentration of melatonin.Clearly, the abrupt and unprecedented onset of darkness (i.e.'night') triggered the SCN which was at once capable of stimulating the pineal gland to secret melatonin.This result offers strong evidence that the link between the SCN and the pineal gland remains uninterrupted in summer.The outstanding question, therefore, is whether the SCN of reindeer sustains circadian rhythmicity in the absence of environmental (photoperiodic) input.Clearly, in mid-summer it cannot owing to the animals' exposure to continuous bright light, but what is the situation in late winter and late summer when the animals are exposed to a daily light/dark cycle?Is it the case that the SCN can sustain a daily rhythm at these times -just as in temperate species of mammals -and that this ability is lost in summer or, alternatively, is the SCN just a passive partner in the system, with its activity being triggered literally every day?Results from a recent series of trials conducted in Tromsø favour the latter model.No evidence has been found of any persistent daily cycle in the secretion of melatonin in reindeer exposed to several days continuous darkness in spring and autumn (K.-A.Stokkan, unpubl.data).Thus far, therefore, it seems possible that the 108 daily rhythm of melatonin secretion in reindeer is generally driven by the daily light/dark cycle and not by an endogenous mechanism.This situation, if confirmed, would be unique among vertebrates.Conclusion Reindeer and muskoxen display a rich variety of daily and annual rhythms in their behaviour and their physiological function which, through accurate timing, ensure that the animals' requirements are adapted to the challenges imposed by the environment.The driving force behind this rhythmicity, however, has as yet not been identified.Remarkably, it is not even certain to what extent the rhythms are driven by endogenous mechanisms.The criteria for identifying circadian rhythmicity have not been met in reindeer.Neither their daily rhythms of activity nor their daily cycle of the secretion of melatonin persist under constant photoperiodic conditions.The rhythms quickly become reestablished on exposing the animals to a light/dark cycle but it is not clear whether this is a result of resetting the phase of an endogenous clock or, instead, merely a passive response to an exogenous rhythm.A few shreds of evidence indicate clock function.For example, the phase of the daily onset and end of activity of free-living reindeer deviates asynchronously from sunrise and sunset both in late-summer and late-winter (van Oort, unpubl.data).Nevertheless, in reindeer, which show a higher degree of synchrony in seasonal timing than probably any other cervid, clock function remains largely unknown.Failure to demonstrate clock function begs many questions.The disappearance of an overt rhythm can be explained in several ways; either as a 'stopping' of the circadian pacemaker, or as an uncoupling of the rhythm from its pacemaker, or as a desynchronisation among the multiplicity of oscillators which control the rhythms (AschofT, 1981; 1986).The endogenous basis of daily and annual rhythms has been clearly established in sevetal species of temperate ungulates and for this reason alone we would expect to find it in reindeer.The most parsimonious interpretation of the evidence to date, therefore, is that the observed arrhythmicity is due to some kind of uncoupling of the clock rather than its 'stopping'.The circadian timing mechanism shows great flexibility in vertebrates.We have already indicated in this review that subtle differences exist along a latitudinal gradient in the ways in which different sub-species of reindeer respond to changes in photoperiod.It is tempting to suggest that the strength of circadian mechanisms varies across a latitudinal gradient in different species of cervids with reindeer, the most northerly, showing the weakest mechanisms rather as Pittendrigh & Takamura (1989) suggested for different sub-species of Drosophila flies.We have emphasised how exposure to continuous photoperiodic conditions places special demands on timing mechanisms and how arctic species, therefore, are of particular interest for the study of biological rhythms.Reindeer, of course, are not the only mammals which live under a continuous photoperiod; subterranean blind mole rats (Spalax ehrenbergi: Goldman et al, 1997) live in constant darkness.Unlike reindeer however, these animals have persistant rhythms, indicating the presence of strong oscillators.Rigid temporal organisation, therefore, remains, even in the absence of temporal information.High arctic reindeer and ptarmigan, however, appear to be released from the grip of the biological clock in summer and winter which enables them, instead, to become truly opportunistic at these times.

Table 1 . Glossary. Terminology Explanation Circadian cycle Entrainment Free-running rhythm Infradian cycle Photoperiod Pineal gland Polar day Polar night SCN Temperature compensation Ultradian cycle Zeitgeber A cycle with a frequency =24 h., i.e. with a length of approximately {circa
-) a day (diem).