Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction

Review Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on Yves Chilliard reproduction François Bocquier, Michel Doreau Laboratoire sous-nutrition des ruminants, Inra, Theix, 63122 Saint-Genès-Champanelle, France (Received 12 February 1998; accepted 2 March 1998) Abstract - In response to undernutrition, short- (days) and medium-term (weeks) adaptations are more pronounced for splanchnic organs than for other tissues. For the latter, the long-term response involves a sequential mobilization (fat > muscle > bone) with relative priorities differing among anatomical sites. Among chemical components, the body lipids are extensively used (up to 80 %) in underfed animals, while the range of protein utilization is limited (up to 15-20 %). The decrease in energy expenditure during undernutrition is mostly due to a short- and medium-term decrease in feeding activity, and in the mass and activity of splanchnic tissues. In the long-term, energy expenditure and tissue masses decrease concomitantly, but there does not appear to be a significant decrease in expenditure per unit tissue weight. Nitrogen losses decrease in response to decline in nitrogen fluxes and also due to sparing by renal activities and sometimes by urea recycling. However, ruminants do not seem to be able to compensate for a low level of intake (below maintenance) by an increase in digestive efficiency. Numerous hormones (insulin, growth hormone, insulin-like growth factor I, catecholamines, thyroid hormones, cortisol, leptin, etc.) are involved in the changes during undernutrition of nutrient fluxes between tissues, either through control of synthesis and/or degradation in peripheral tissues (adipose tissue and muscle), or through hepatic conversions of substrates (gluconeogenesis, ureagenesis and ketogenesis), in order to maintain the constancy of the internal environment (homeostasis) and/or to sustain productive functions (teleophoresis). However, reproductive process may be blocked in underfed animals. © Inra/Elsevier, Paris body reserves / digestion / hormones / metabolism / reproduction / ruminants / undemutrition Résumé - Adaptations digestives et métaboliques des ruminants à la sous-nutrition. Conséquences sur la reproduction. En réponse à une sous-nutrition, les adaptations à court terme (jours) ou à moyen terme (semaines) sont plus importantes pour les tissus splanchniques que * Correspondence and reprints E-mail: pour les autres tissus. On observe à long terme une mobilisation tissulaire séquentielle (gras > muscle > os), avec des priorités variables entre sites anatomiques. Parmi les constituants chimiques, les lipides corporels sont largement utilisés (jusqu’à 80 %) chez les animaux sous-nutris, alors que les protéines corporelles sont moins sollicitées (jusqu’à 15-20 %). La diminution de la dépense énergétique pendant la sous-nutrition est principalement due, à court et moyen terme, à des réductions des activités alimentaires et de la masse et de l’activité des tissus splanchniques. A long terme, la dépense énergétique diminue parallèlement à celle de la masse corporelle, et il ne semble pas y avoir de diminution significative de la dépense par gramme de tissu. La dépense azotée est diminuée parallèlement à la réduction des flux d’azote, mais également par une économie au niveau du rein et parfois par un recyclage de l’urée. Toutefois, les ruminants ne semblent pas pouvoir compenser une diminution du niveau d’ingestion (en dessous de l’entretien) par une meilleure efficacité digestive. De nombreuses hormones (insuline, hormone de croissance, IGF-1, catécholamines, hormones thyroïdiennes, cortisol, leptine,..) sont impliquées dans les modifications des flux de nutriments entre tissus causées par la sous-nutrition. Elles agissent en régulant soit les synthèses, soit les dégradations au niveau des tissus périphériques (tissu adipeux, muscle), ou les transformations hépatiques des substrats (pour la néoglucogenèse, l’uréogenèse et la cétogenèse), pour maintenir la constance du milieu intérieur (homéostasie) ou pour soutenir des fonctions productives (téléophorèse). Toutefois, la fonction de reproduction peut être bloquée par la sous-nutrition. @ Inra/Elsevier, Paris digestion / hormones / métabolisme / reproduction / réserves corporelles / ruminants / sous-nutrition 1. INTRODUCTION The ability of ruminants to cope with periods of food shortage is the result of a long evolutionary process in natural conditions where food availability seasonally fluctuates. Most domesticated ruminants are subject to major constraints, some of which are reinforced by man who utilizes their adaptability for economic or husbandry reasons. For example, beef cows are often underfed in winter, when the availability of conserved forages is limited; they restore their body reserves at pasture. Group-fed ewes can also be underfed when food supply is given according to the average requirements of the group, owing to variability in their requirements. Besides this, physiological underfeeding is the general rule of high producing dairy cows in early lactation. However, the most drastic problems of underfeeding occur because of unfavourable climatic conditions which limit forage growth and thus availability, especially in arid and tropical areas. In such situations, all the coping mechanisms and especially body fat and protein mobilisation strategies are obviously of considerable importance in determining animal productivity and, in many instances, survival. This paper describes the adaptative mechanisms of digestion and metabolism in underfed ruminants. The central role of body reserves is considered together with variations in maintenance (M) expenditures in non-productive animals. In productive animals, interactions between nutrition and physiological demand for reproduction, pregnancy, lactation or growth have been used to highlight adaptative mechanisms involved when food supply is inadequate. Indeed, even if food supply is abundant and constant, changes in nutrient demand may also create unbalanced nutritional situations, thus leading to a distinction between absolute and relative inadequacy of food supply. We have also made distinctions between different time-scales in adaptations to food supply: short-term adaptation (d) due to diurnal feeding frequency or from day-to-day changes in food availability; medium-term adaptations that appear within a few weeks; and long-term adaptations that require animals to progress towards a new equilibrium in a different nutritional and/or physiological context. 2. VARIATIONS IN BODY WEIGHT AND COMPOSITION When ruminants are underfed, shortterm decreases in live weight (LW) are due mainly to gut fill variations (-4 to -5 kg LW per kg decrease in dry matter intake). When intake is stabilized (medium term), however, LW variations mostly reflect changes in organ and tissue masses. In the case of severe undernutrition of Lacaune ewes ( (...truncated)