Our study clearly shows that Tb of female muskoxen in the high Arctic varies markedly across the year, and some females displayed lowered body temperature during periods of resource scarcity. This suggests that muskoxen can adopt hypothermia as an over-wintering strategy to conserve energy. Body temperature and metabolic rate generally correlates well across vertebrate species24 and within individuals25,26 (but not always27), and hypothermia may thus be indicative of hypometabolism. Both hypothermia and hypometabolism have previously been reported for a variety of mammal species1,3, including high latitude ungulates5, as adaptations to the annual cycle in seasonal environments. However, and more importantly, we revealed a link between Tb, activity level, and pregnancy status in muskoxen. Without further study we cannot untangle whether these differences in Tb, and thus likely differences in metabolic rates, are caused by the reproductive status of the female or vice versa, highlighting an important gap in current knowledge that needs further study. Regardless, the differences in Tb between pregnant and non-pregnant muskoxen likely result in substantially different metabolic costs28.
As hypothesized, pregnant females that carried their foetus to term exhibited a high degree of homeothermy during the gestation period. This pattern resembles that observed in other mammals, such as bears13. However, while Thiel et al.11 also reported more stable Tb in pregnant wolverines as compared to non-pregnant ones, they found that wolverines lowered their Tb during gestation. These contrasting reports suggest that the use of hypothermia as an over-winter strategy during pregnancy likely depends on species-specific life-history traits, for instance body mass and whether a given species relies on accumulated reserves or continues feeding during gestation. Indeed, in addition to environmental conditions, the degree of heterothermy in mammal species is linked to their evolutionary history29.
We observed remarkably similar mean daily Tb (and its range) for both captive and wild pregnant muskoxen, despite clear differences in food availability, ambient temperature and snow conditions (Fig. 1). This finding suggests that both groups of pregnant females had sufficient energy reserves to sustain somatic maintenance and foetal growth without lowering their core Tb, whilst also providing thermal protection for the developing foetus30 during the cold arctic winter. Though these reproductively successful wild females were generally the least active in winter compared to the other wild muskoxen, differences were not pronounced and therefore only marginal differences in energy expenditure are to be expected. Nonetheless, the lower activity levels may be seen as a general energy conserving strategy but also indicative of lower need for foraging and relocation activities in winter, further supporting that these individuals were in better condition in winter as compared to the other wild muskoxen, enabling them to both survive and cover gestational costs.
Activity levels and Tb of wild non-pregnant muskoxen increased steadily after the winter nadir until mid-summer, where Tb reached levels above those observed the previous autumn for any of the muskox groups. This pattern likely reflects increased foraging activities in the summer season to replenish energy reserves31. The surviving non-pregnant females all had a calf at heel in the autumn and had thus been nursing the young in the summer before collaring. These females had slightly lower Tb compared to both wild and captive reproducing females already in late autumn, and thus already exhibited signs of hypothermia. Whilst the reduction in Tb was quite small, this may indicate that these females had insufficient body reserves in autumn to support oestrus, likely due to the high energetic costs of lactation for the calf at heel32. In muskoxen, lactation does not preclude pregnancy, but appears limited to those in better body condition18. Interestingly, one year after collaring, Tb levels of females that were non-pregnant in autumn 2017 reached Tb levels of pregnant females. These patterns support previous findings that the high costs associated with pregnancy and lactation32 may lead to alternate year breeding in wild muskoxen in northeast Greenland23. However, at the time of collaring, the non-pregnant muskoxen were the heaviest among the wild muskoxen (Table 1), suggesting that body mass alone is not the sole determinant of oestrus and that a physiological postpartum (lactational) anoestrus33 may contribute to the observed pregnancy patterns.
For both groups of non-reproducing muskoxen in the wild, the rapid Tb decline may indicate a starvation-induced temperature drop, as similar Tb signatures have been found in other starving animals28, including ungulates34. However, in contrast to the surviving non-reproducing females, females that eventually died did not manage to reverse the negative temperature development in late winter, and the late drop in Tb can be seen as a stress response to severe energy depletion. Though it was evident in all wild muskox groups that daily Tb ranges increased during the course of winter, likely induced by energy deficiency35, the muskoxen that eventually died exhibited the most dramatic loss of homeothermy with the largest and rapidly increasing daily Tb ranges during winter.
In this study we have shown that Tb of some muskox females decreased during winter, indicating the use of hypothermia, and potentially also hypometabolism, during the resource-poor and harsh high arctic winter. However, this physiological energy conservation strategy appears restricted to females that do not (successfully) reproduce. Hypothermia may limit overwinter depletion of energy stores and subsequently allow these individuals to reproduce the following year. However, in endothermic animals where Tb is generally regulated within a narrow range, heterothermy may come at a cost. In rabbits (Oryctolagus cuniculus), increased daily heterothermy resulted in reduced future fitness in terms of fewer litters born35. Whether such fitness cost is applicable to other species, such as the muskox, is not known. Interestingly, muskoxen living in more productive areas than high arctic Greenland, may have successive year breeding23, indicating that metabolic strategies may be flexible in muskoxen, with hypothermia limited to individuals living in areas with severe energetic constraints in winter, and where current survival may outweigh future fitness costs.
Despite our limited sample size, we posit that the link between reproduction and hypothermia as an overwintering strategy may be due to a trade-off between the need to reduce metabolic costs and the need to maintain foetal growth. We advocate that an intimate link between energy reserves and reproductive status may exists, at least in muskox females32 under severe energetic constraints, which can have subsequent consequences on individual energy balance and ultimately population dynamics. While our study has provided the first indications of such a relationship in a wild, large herbivorous mammal, we emphasise that more studies on the linkage between animal Tb, metabolism and pregnancy, particularly from highly seasonal environments, are needed to further support our claims. Understanding individual energy balances in species occupying highly seasonal environments is a prerequisite for assessing how populations may cope with current and future changes in climatic conditions.
Source: Ecology - nature.com
