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Review: Seasonal differences in the physiology of wild northern ruminants

  • W. Arnold (a1)

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.

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References

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Arnold, W, Beiglböck, C, Burmester, M, Guschlbauer, M, Lengauer, A, Schröder, B, Wilkens, M and Breves, G 2015b. Contrary seasonal changes of rates of nutrient uptake, organ mass, and voluntary food intake in red deer (Cervus elaphus). American Journal of Physiology – Regulatory and Integrative Comparative Physiology 309, R277R285.
Arnold, W, Giroud, S, Valencak, TG and Ruf, T 2015a. Ecophysiology of omega fatty acids: a lid for every jar. Physiology 30, 232240.
Arnold, W, Ruf, T and Kuntz, R 2006. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy expenditure. Journal of Experimental Biology 209, 45664573.
Arnold, W, Ruf, T, Loe, LE, Irvine, RJ, Ropstad, E, Veiberg, V and Albon, SD 2018. Circadian rhythmicity persists through the Polar night and midnight sun in Svalbard reindeer. Scientific Reports 8, 14466.
Arnold, W, Ruf, T, Reimoser, S, Tataruch, F, Onderscheka, K and Schober, F 2004. Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus). American Journal of Physiology – Regulatory and Integrative Comparative Physiology 286, R174R181.
Aschenbach, JR, Penner, GB, Stumpff, F and Gäbel, G 2011. Ruminant Nutrition Symposium: role of fermentation acid absorption in the regulation of ruminal pH. Journal of Animal Science 89, 10921107.
Barboza, PS, Peltier, TC and Forster, RJ 2006. Ruminal fermentation and fill change with season in an arctic grazer: responses to hyperphagia and hypophagia in muskoxen (Ovibos moschatus). Physiological and Biochemical Zoology 79, 497513.
Beatty, DT, Barnes, A, Taylor, E and Maloney, SK 2008. Do changes in feed intake or ambient temperature cause changes in cattle rumen temperature relative to core temperature? Journal of Thermal Biology 33, 1219.
Breves, G and Schröder, B 1991. Comparative aspects of gastrointestinal phosphorus metabolism. Nutrition Research Reviews 4, 125140.
Brinkmann, L, Gerken, M and Riek, A 2012. Adaptation strategies to seasonal changes in environmental conditions of a domesticated horse breed, the Shetland pony (Equus ferus caballus). The Journal of Experimental Biology 215, 10611068.
Brinkmann, L, Riek, A and Gerken, M 2017. Long-term adaptation capacity of ponies: effect of season and feed restriction on blood and physiological parameters. Animal 12, 8897.
Crater, AR and Barboza, PS 2007. The rumen in winter: cold shocks in naturally feeding muskoxen (Ovibos moschatus). Journal of Mammalogy 88, 625631.
Crater, AR, Barboza, PS and Forster, RJ 2007. Regulation of rumen fermentation during seasonal fluctuations in food intake of muskoxen. Comparative Biochemistry and Physiology A-Molecular and Integrative Physiology 146, 233241.
DelGiudice, GD, Mech, LD, Kunkel, KE, Gese, EM and Seal, US 1992. Seasonal patterns of weight, hematology, and serum characteristics of free-ranging female deer in Minnesota. Canadian Journal of Zoology 70, 974983.
Durand, M and Kawashima, R 1980. Influence of minerals in rumen microbial digestion. In Digestive physiology and metabolism in ruminants: proceedings of the 5th international symposium on ruminant physiology, held at Clermont-Ferrand, on 3rd–7th September, 1979 (ed. Ruckebusch, Y and Thivend, P), pp. 375408. Springer Netherlands, Dordrecht.
Ferraris, RP and Carey, HV 2000. Intestinal transport during fasting and malnutrition. Annual Review of Nutrition 20, 195219.
Geiser, F and Ruf, T 1995. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiological Zoology 68, 935966.
Giacometti, M, Bassano, B, Peracino, V and Ratti, P 1997. Die Konstitution des Alpensteinbockes (Capra i. ibex L.) in Abhängigkeit von Geschlecht, Alter, Herkunft und Jahreszeit in Graubünden (Schweiz) und im Parco Nazionale Gran Paradiso (Italien). Zeitschrift für Jagdwissenschaft 43, 2434.
Heydon, MJ, Sibbald, AM, Milne, JA, Brinklow, BR and Loudon, ASI 1993. The interaction of food availability and endogenous physiological cycles on the grazing ecology of red deer hinds (Cervus elaphus). Functional Ecology 7, 216222.
Hofmann, RR 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443457.
Holand, Ø 1994. Seasonal dynamics of digestion in relation to diet quality and intake in European roe deer (Capreolus capreolus). Oecologia 98, 274279.
Huber, K, Roesler, U, Muscher, A, Hansen, K, Widiyono, I, Pfeffer, E and Breves, G 2003. Ontogenesis of epithelial phosphate transport systems in goats. American Journal of Physiology – Regulatory and Integrative Comparative Physiology 284, R413R421.
Huber, K, Walter, C, Schröder, B and Breves, G 2002. Phosphate transport in the duodenum and jejunum of goats and its adaptation by dietary phosphate and calcium. American Journal of Physiology – Regulatory and Integrative Comparative Physiology 283, R296R302.
Hume, ID 1989. Optimal digestive strategies in mammalian herbivores. Physiological Zoology 62, 11451163.
Hume, ID, Beiglböck, C, Ruf, T, Frey-Roos, F, Bruns, U and Arnold, W 2002. Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). Journal of Comparative Physiology B: Biochemical Systemic and Environmental Physiology 172, 197207.
Irving, L and Krog, J 1955. Temperature of skin in the arctic as a regulator of heat. Journal of Applied Physiology 7, 355364.
Knott, KK, Barboza, PS and Bowyer, RT 2005. Growth in Arctic ungulates: postnatal development and organ maturation in Rangifer tarandus and Ovibos moschatus. Journal of Mammalogy 86, 121130.
Kuntz, R, Kubalek, C, Ruf, T, Tataruch, F and Arnold, W 2006. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) I. Energy intake. The Journal of Experimental Biology 209, 45574565.
Lawler, JP and White, RG 2003. Temporal responses in energy expenditure and respiratory quotient following feeding in the muskox: influence of season on energy costs of eating and standing and an endogenous heat increment. Canadian Journal of Zoology 81, 15241538.
Lechner-Doll, M, Kaske, M and von Engelhardt, W 1991. Factors affecting the mean retention time of particles in the forestomach of rumiants and camelids. In Physiological aspects of digestion and metabolism in ruminants (ed. Tsuda, T, Sasaki, Y and Kawashima, R), pp. 455482. Academic Press, London, UK.
Lincoln, GA, Andersson, H and Loudon, A 2003. Clock genes in calendar cells as the basis of annual timekeeping in mammals – a unifying hypothesis. Journal of Endocrinology 179, 113.
Loudon, ASI 1994. Photoperiod and the regulation of annual and circannual cycles of food intake. Proceedings of the Nutrition Society 53, 495507.
Milner, JM, Beest, FM, Solberg, EJ and Storaas, T 2012. Reproductive success and failure: the role of winter body mass in reproductive allocation in Norwegian moose. Oecologia, 111.
Parker, KL, Gillingham, MP, Hanley, TA and Robbins, CT 1993. Seasonal patterns in body mass, body composition, and water transfer rates of free-ranging and captive black-tailed deer in Alaska. Canadian Journal of Zoology 71, 13971404.
Pelletier, F, Réale, D, Grant, D, Coltman, DW and Festa-Bianchet, M 2011. Selection on heritable seasonal phenotypic plasticity of body mass. Evolution 61, 19691979.
Peltier, TC and Barboza, PS 2003. Growth in an arctic grazer: effects of sex and dietary nitrogen on yearling muskoxen. Journal of Mammalogy 84, 915925.
Peltier, TC, Barboza, PS and Blake, JE 2003. Seasonal hyperphagia does not reduce digestive efficiency in an Arctic Grazer. Physiological and Biochemical Zoology 76, 471483.
Reimoser, S 2012. Influence of anthropogenic disturbance on activity, behaviour and heart rate of roe deer (Capreolus capreaolus) and red deer (Cervus elaphus), in context of their daily and yearly patterns. In Deer: habitat, behaviour and conservation (ed. Cahler, AA), pp. 195. Nova Science Publishers, Hauppauge, NY, USA.
Riek, A, Brinkmann, L, Gauly, M, Perica, J, Ruf, T, Arnold, W, Hambly, C, Speakman, JR and Gerken, M 2017. Seasonal changes in energy expenditure, body temperature and activity patterns in llamas (Lama glama). Scientific Reports 7, 7600.
Rutley, BD and Hudson, RJ 2000. Seasonal energetic parameters of free-grazing bison (Bison bison). Canadian Journal of Animal Science 80, 663671.
Scholander, PF, Hock, R, Walters, V, Johnson, F and Irving, L 1950. Heat regulation in some arctic and tropical mammals and birds. Biological Bulletin 99, 237258.
Short, HL, Medin, E and Anderson, AE 1966. Seasonal variations in volatile fatty acids in the Rumen of Mule Deer. The Journal of Wildlife Management 30, 466470.
Signer, C, Ruf, T and Arnold, W 2011. Hypometabolism and basking: the strategies of Alpine ibex to endure harsh over-wintering conditions. Functional Ecology 25, 537547.
Stevens, EC and Hume, ID 1995. Comparative physiology of the vertebrate digestive system. Cambridge University Press, N.Y., Melbourne, Australia.
Stokstad, E 2015. Bringing back the aurochs. Science 350, 11441147.
Tataruch, F and Onderscheka, K 1993. Gehalt an Ammoniak und flüchtigen Fettsäuren im Pansensaft von Rot-, Reh- und Gamswild. Wiener Tierärztliche Monatsschrift 80, 269274.
Tataruch, F and Onderscheka, K 1996. Chemische Analysen der Panseninhalte von Steinwild in Graubünden. Zeitschrift für Jagdwissenschaft 42, 1825.
Thompson, DP, Barboza, PS, Crouse, JA, McDonough, TJ, Badajos, OH and Herberg, AM 2019. Body temperature patterns vary with day, season, and body condition of moose (Alces alces). Journal of Mammalogy, 113.
Turbill, C, Ruf, T, Mang, T and Arnold, W 2011. Regulation of heart rate and rumen temperature in red deer: effects of season and food intake. Journal of Experimental Biology 214, 963970.
Tyler, NJC and Blix, AS 1990. Survival strategies in arctic ungulates. Rangifer Special Issue 3, 211230.
Wascher, CAF, Kotrschal, K and Arnold, W 2018. Free-living greylag geese adjust their heart rates and body core temperatures to season and reproductive context. Scientific Reports 8, 2142.
Weiss, CP, Gentry, WW, Meredith, CM, Meyer, BE, Cole, NA, Tedeschi, LO, McCollum, FT III and Jennings, JS 2017. Effects of roughage inclusion and particle size on digestion and ruminal fermentation characteristics of beef steers. Journal of Animal Science 95, 17071714.

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Review: Seasonal differences in the physiology of wild northern ruminants

  • W. Arnold (a1)

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