Review: Seasonal differences in the physiology of wild northern ruminants

Abstract

Ruminants living in seasonal environments face a two-fold challenge during winter. The energetic cost of maintaining a high body temperature is higher at lower ambient temperatures, and this is compounded by poor availability and quality of feed. Wild ruminants acclimatize to this energetic challenge by hypothermia, that is, reduced endogenous heat production and abandoning the maintenance of a high body temperature, particularly in peripheral body parts. Further but lesser contributions to lower energy expenditure during winter are reduced foraging activity; lower heat increment of feeding; and reduced maintenance cost of size-reduced organs. Altogether, metabolic rate, estimated by the continuous measurement of heart rate, during winter is downregulated to more than half of the summer level, as is voluntary food intake, even in animals fed ad libitum. The transformation from the summer into the thrifty winter phenotype is also evident in the physiology of digestion. Microbial protein synthesis is less facilitated by diminished phosphorus secretion into the shrunk rumen during winter. In line with this result, the concentration of ammonia, the end-product of protein digestion in the rumen, peaks in rumen liquid in spring, whereas the molar proportion of acetate, an indicator of fermentation of a diet rich in fiber, peaks in winter. In contrast to reduced stimulation of growth of ruminal microbes during winter, active transport of nutrients across the intestinal epithelium is increased, resulting in more efficient exploitation of the lower amount and quality of ingested winter feed. Nevertheless, the energy balance remains negative during winter. This is compensated by using fat reserves accumulated during summer, which become a major metabolic fuel during winter.

Determinants of heart rate in Svalbard reindeer reveal mechanisms of seasonal energy management

“…Overall, the strong seasonal pattern in heart rate contributes to the increasing evidence that seasonal animals upregulate energy expenditure in periods of high supply and downregulate it when food is scarce [ 22 – 24 ]. The relatively small elevations in heart rate in lactating females could indicate that breeding female reindeer are close to their upper limits of sustained metabolic rate in summer.…”

“…The most pronounced temporal reductions in energy expenditure are observed in species exhibiting daily torpor and hibernation, characterized by substantially lowered metabolic rate, body temperature and reduced movement [ 19 ]. However, accumulating evidence shows that many non-hibernating temperate animals also display seasonal adjustments in metabolic rate [ 20 – 23 ] through reduced body temperature and activity levels [ 24 – 26 ]. Similar responses have been observed in desert ungulates during the hot, dry season when food is limited [ 27 – 29 ].…”

A unifying, eco‐physiological framework for animal dormancy

“…Dormancies have been documented in all animal phyla except Echinodermata (Hand, 1991), and are described using a wide variety of taxon‐specific names and definitions (Table 1). Within and among these groups, dormancies span an extremely broad range of physiological states, from the nearly inert, ‘latent life’ state called cryptobiosis exemplified by Tardigrades (Jönsson et al., 2019) to more subtle state of hypometabolism exhibited by some active high latitude ungulates (in winter; Arnold, 2020) and polar bears (in summer; Nelson et al., 1983; Whiteman et al., 2015).…”

Fat storage influences fasting endurance more than body size in an ungulate

“…Many ungulates display pronounced seasonal adjustments in locomotor activity, body temperature and energy expenditure (reviewed in Arnold, 2020), which is also evident for Svalbard reindeer (Trondrud, Pigeon, Albon, et al., 2021). We found that adjustments in T sc and activity levels can alter the FE of Svalbard reindeer by up to 20% if both parameters are reduced at the same time.…”