Microanatomy of incremental growth lines in dental tissues in reindeer Rangifer tarandus.

Counting growth layers in dentine and/or secondary cementum is widely used for age determination in wild mammals but the underlying seasonal changes in the structure and degree of mineralisation of dental tissue have not been well characterised. We embedded first (m1) and second (m2) mandibular permanent molar teeth from a 12-year-old female Svalbard reindeer (Rangifer tarandus platyrhynchus) in PolyMethylMethAcrylate (PMMA), prepared cut and polished surfaces coated with evaporated carbon and used 20 kV back-scattered electron imaging in a scanning electron microscope (BSE-SEM) to study aspects of dental tissue structure which depend on the degree of mineralisation at the micron and sub-micron scale. BSE-SEM revealed differences between the mineral content of growth layers (annulations) in the secondary cementum and the primary and secondary dentine, the latter, incidentally, still forming at death in m1. Wide bands of less well mineralised tissue formed in the cementum during active appositional phases. Thin, denser bands formed by maturation-mineralisation of existing tissue when growth slowed in winter. This maturation mimics the processes seen in lamellar bone and articular cartilage. Counter to previous suggestions, there was evidence of substantial resorption and repair of the secondary cementum and of formation of dentine throughout life. Secondary dentine is layered by mineral content like cementum. In the crown, this was mainly tubular dentine with well-marked interglobular dentine layers. In the lower pulp chamber and root, it was largely without tubules. Substantial non-mineralised spaces found at the cement-dentine junction in the root apical regions in m2 represent inclusions of the Hertwig's Epithelial Root Sheath (HERS) or the Epithelial Rests of Malassez (ERM) between the two tissues, a phenomenon which has previously only been identified in Muridae. The anatomical changes which result in the formation of the incremental lines (annulations) in dental tissues of reindeer, identified here for the first time at the micrometre level, are likely to be common across most if not all long-lived species of mammals living in seasonal environments.

Activity patterns in mammals: Circadian dominance challenged.

The evidence that diel patterns of physiology and behaviour in mammals are governed by circadian 'clocks' is based almost entirely on studies of nocturnal rodents. The emergent circadian paradigm, however, neglects the roles of energy metabolism and alimentary function (feeding and digestion) as determinants of activity pattern. The temporal control of activity varies widely across taxa, and ungulates, microtine rodents, and insectivores provide examples in which circadian timekeeping is vestigial. The nocturnal rodent/human paradigm of circadian organisation is unhelpful when considering the broader manifestation of activity patterns in mammals.

Circadian organization in reindeer.

The light/dark cycle of day and night synchronizes an internal 'biological clock' that governs daily rhythms in behaviour, but this form of regulation is denied to polar animals for most of the year. Here we demonstrate that the continuous lighting conditions of summer and of winter at high latitudes cause a loss in daily rhythmic activity in reindeer living far above the Arctic Circle. This seasonal absence of circadian rhythmicity may be a ubiquitous trait among resident polar vertebrates.

Nonlinear effects of climate and density in the dynamics of a fluctuating population of reindeer.

Nonlinear and irregular population dynamics may arise as a result of phase dependence and coexistence of multiple attractors. Here we explore effects of climate and density in the dynamics of a highly fluctuating population of wild reindeer (Rangifer tarandus platyrhynchus) on Svalbard observed over a period of 29 years. Time series analyses revealed that density dependence and the effects of local climate (measured as the degree of ablation [melting] of snow during winter) on numbers were both highly nonlinear: direct negative density dependence was found when the population was growing (Rt > 0) and during phases of the North Atlantic Oscillation (NAO) characterized by winters with generally high (1979-1995) and low (1996-2007) indices, respectively. A growth-phase-dependent model explained the dynamics of the population best and revealed the influence of density-independent processes on numbers that a linear autoregressive model missed altogether. In particular, the abundance of reindeer was enhanced by ablation during phases of growth (Rt > 0), an observation that contrasts with the view that periods of mild weather in winter are normally deleterious for reindeer owing to icing of the snowpack. Analyses of vital rates corroborated the nonlinearity described in the population time series and showed that both starvation mortality in winter and fecundity were nonlinearly related to fluctuations in density and the level of ablation. The erratic pattern of growth of the population of reindeer in Adventdalen seems, therefore, to result from a combination of the effects of nonlinear density dependence, strong density-dependent mortality, and variable density independence related to ablation in winter.

Behavioral Timing without Clockwork: Photoperiod-Dependent Trade-Off between Predation Hazard and Energy Balance in an Arctic Ungulate.

Occurrence of 24-h rhythms in species apparently lacking functional molecular clockwork indicates that strong circadian mechanisms are not essential prerequisites of robust timing, and that rhythmical patterns may arise instead as passive responses to periodically changing environmental stimuli. Thus, in a new synthesis of grazing in a ruminant (MINDY), crepuscular peaks of activity emerge from interactions between internal and external stimuli that influence motivation to feed, and the influence of the light/dark cycle is mediated through the effect of low nocturnal levels of food intake on gastric function. Drawing on risk allocation theory, we hypothesized that the timing of behavior in ruminants is influenced by the independent effects of light on motivation to feed and perceived risk of predation. We predicted that the antithetical relationship between these 2 drivers would vary with photoperiod, resulting in a systematic shift in the phase of activity relative to the solar cycle across the year. This prediction was formalized in a model in which phase of activity emerges from a photoperiod-dependent trade-off between food and safety. We tested this model using data on the temporal pattern of activity in reindeer/caribou Rangifer tarandus free-living at natural mountain pasture in sub-Arctic Norway. The resulting nonlinear relationship between the phasing of crepuscular activity and photoperiod, consistent with the model, suggests a mechanism for behavioral timing that is independent of the core circadian system. We anticipate that such timing depends on integration of metabolic feedback from the digestive system and the activity of the glucocorticoid axis which modulates the behavioral responses of the animal to environmental hazard. The hypothalamus is the obvious neural substrate to achieve this integration.

A circadian clock is not required in an arctic mammal.

Seasonally breeding mammals use the annual change in the photoperiod cycle to drive rhythmic nocturnal melatonin signals from the pineal gland, providing a critical cue to time seasonal reproduction. Paradoxically, species resident at high latitudes achieve tight regulation of the temporal pattern of growth and reproduction despite the absence of photoperiodic information for most of the year. In this study, we show that the melatonin rhythm of reindeer (Rangifer tarandus) is acutely responsive to the light/dark cycle but not to circadian phase, and also that two key clock genes monitored in reindeer fibroblast cells display little, if any, circadian rhythmicity. The molecular clockwork that normally drives cellular circadian rhythms is evidently weak or even absent in this species, and instead, melatonin-mediated seasonal timing may be driven directly by photic information received at a limited time of year specific to the equinoxes.

Ecological dynamics across the Arctic associated with recent climate change.

At the close of the Fourth International Polar Year, we take stock of the ecological consequences of recent climate change in the Arctic, focusing on effects at population, community, and ecosystem scales. Despite the buffering effect of landscape heterogeneity, Arctic ecosystems and the trophic relationships that structure them have been severely perturbed. These rapid changes may be a bellwether of changes to come at lower latitudes and have the potential to affect ecosystem services related to natural resources, food production, climate regulation, and cultural integrity. We highlight areas of ecological research that deserve priority as the Arctic continues to warm.

Adaptations for life in the Arctic: evidence that melatonin rhythms in reindeer are not driven by a circadian oscillator but remain acutely sensitive to environmental photoperiod.

In reindeer Rangifer tarandus, a high latitude species, the rhythmic production of melatonin periodically dissipates under natural photoperiods when, in mid-winter, there is near permanent darkness and again, in summer, when there is permanent light. In spring and autumn, as expected, melatonin production reflects the ambient light:dark (LD) cycle. We investigated the expression of circadian mechanisms on blood levels of melatonin in reindeer. Two experiments were conducted in which animals were transferred from natural photic conditions into continuous darkness for 3 days: (i) in February, when they had been exposed to an LD cycle (11L:13D) and (ii) in July, when they had been exposed to permanent light. In July, plasma levels of melatonin rose abruptly on exposure to darkness but then declined over 24 hr before displaying a second rise and decline over the following 36 hr. In contrast, in February, levels of melatonin rose abruptly but then remained elevated for more than 60 hr in darkness. Melatonin secretion upon exposure to darkness did not conform to a circadian pattern and did not, therefore, support the hypothesis that pineal activity in reindeer is tightly regulated by circadian mechanisms. Instead the secretion of melatonin appeared to be acutely and directly sensitive to ambient lighting. The results are consistent with a model in which Arctic resident animals have adapted to extreme photic conditions by disconnecting the generation of the pineal melatonin signal from their circadian machinery and relying, instead, on its being driven by the LD cycle for just a few weeks annually in spring and autumn.

Where clocks are redundant: weak circadian mechanisms in reindeer living under polar photic conditions.

Biological rhythms are a result of interplay between endogenous clocks and the ambient light-dark (LD) cycle. Biological timing in resident polar organisms presents a conundrum because these experience distinct daily LD cycles for only a few weeks each year. We measured locomotor activity in reindeer, Rangifer tarandus platyrhynchus (SR, n = 5 and 6) and R. tarandus tarandus (NR, n = 6), ranging freely at 78 and 70 degrees N, respectively, continuously throughout 1 year using data loggers. NR, but not SR, are gregarious which enabled us to examine the integrated effects of differences in social organisation and the photic environment at two different latitudes on the organisation of activity. In both sub-species, ultradian bouts of activity and inactivity alternated across the 24-h day throughout the year. This pattern was modified by the LD cycle in NR but barely at all in SR. Periodogram analysis revealed significant ultradian rhythmicity in both sub-species; the frequency of daily cycles of activity increased from three per day in winter to nearly five in summer. We conclude that this increase, and a concomitant increase in the level of daily activity, reflected the seasonal increase in the animals' appetite and the quality of their forage. Secondly, the combination, most evident in SR, of a weak photic response, weak circadian mechanisms and a weak social synchronization reduces the constraints of biological timing in an environment which is effectively non-rhythmic most of the year and permits expression of the basic ultradian pattern of ruminant activity. Third, the weaker 24-h rhythmicity in SR compared to NR indicates a latitudinal decrease in circadian organization and photic responsiveness in Rangifer.