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Relationships between hormone-induced and compensatory weight changes in reindeer (Rangifer tarandus tarandus)
Cwyp. Biochm. Pkysid. Vol. 74A. No. I. pp. 3.1 to 35. 1983 Printed in Great Britain.
0300.9h29,;83i01033-03~3.00~0 0 1983 Pergnmon Press Ltd
RELATIONSHIPS BETWEEN HORMONE-INDUCED AND COMPENSATORY WEIGHT CHANGES IN REINDEER (RANGIFER TARANDUS TARANDUS) MORTEN
Institute
of
Zoophysiology,
RYG
University of Oslo, P.O. Box 1031 Blindern. Oslo 3, Norway (Received
30 March
1982)
Abstract-l. In connection with a study of hormonal effects on food consumption in reindeer, weight changes during treatment were compared with weight changes during a 3-week period following treatment. 2. Rates of weight change during the post-treatment period were inversely proportional to induced weight changes. 3. This inverse relationship is interpreted as evidence for a functional set-point for body weight in reindeer.
INTRODUCTION
Most models considering food intake are based on the assumptions of control of energy balance or maintenance of a stable body weight. However, in a number of species, including many northern ruminants, body weight is not stable, but oscillates between maximal levels in autumn and minima1 levels in spring (McEwan, 1975). This pattern is maintained also with free access to food, and raises the question of how food intake is regulated in these species. Eriksson et al. (198 1) suggested that food intake of reindeer is primarily regulated by the effect of daylength on an ultradian feeding rhythm, with little reference to physiological control. Also, Verme & Ozoga (1980) found that dry matter intake of white-tailed fawns in autumn was little affected by the energy content of the feed. In contrast, Amman et al. (1973) found that digestible energy intake of white-tailed deer fawns in winter was constant when a concentrate diet was progressively diluted with sawdust, as long as digestibility was above 50%. In the present paper, a set-point for body weight is considered as a possible control mechanism. Compensatory weight changes following periods of force-feeding or reduced food access is taken as evidence for a set-point, although the term is often used in a functional sense, and do not necessarily imply the existence of an actual reference signal (Mrosovsky & Powley, 1977). Although similar mechanisms have also been suggested for domestic ruminants (Baile & Forbes, 1974), studies involving fasting in ruminants is complicated by the large and variable gastrointestinal volume of these animals. In connection with an investigation of effects of thyroid hormones and prolactin on reindeer, posttreatment weight changes were compared with weight changes during treatment. Although opposite in their effects on weight gain, these hormones all caused increased food intake, thus probably excluding bias due to filling the rumen during the post-treatment period. If there is a defended body weight. one would expect
that the rate of weight change in the post-treatment period should be inversely related to the induced weight change. MATERIALS
AND
METHODS
The keeping of animals, and hormone treatment, has been described elsewhere (Ryg & Jacobsen, 1982a), Briefly, in three experiments, a total of 24 yearling reindeer bulls were treated with thyroid hormones Il.0 mg triiodothyronine (Sigma T-2877) or 1.2 mg triiodothyronine and 2.4 mg thyroxine (Sigma T-2376) per day], or prolactin [I70 or 250 i.u. ovine prolactin (Sigma L-4876) per day] for 2-4 weeks. The animals were fed a pelleted reindeer feed (RF 71) containing 13.7% protein. 7.2% fat, 62.4% nitrogen-free extracts, 11% crude fiber, and 5.7% ash. Food intake and body weight was recorded during the hormone treatment and a following 3-week period. RESULTS
During the post-treatment period, individual rates of weight change were negatively correlated (r = 0.83, P < 0.01) with the weight changes during the treatment period (Fig. 1). The induced weight change of each animal is expressed as the difference between total weight change in the treatment period and the mean change of the control animals in each experiment. Weight changes in the post-treatment period were significantly correlated with dry matter intake (r = 0.76, P < 0.01) (Fig. 2). For a given dry matter intake, weight gain in animals previously treated with prolactin tended to be lower than in controls. DISCUSSION
Residual effects of the hormone treatment could possibly explain some of the differences in the posttreatment period, especially in animals treated with thyroid hormones. The biological halftime of triiodothyronine in humans is about 1 day (Ingbar & Woeber, 1974) and in yearling reindeer, the halftime of thyroxine is about 3 days (Yousef & Luick, 1971).
MORTEN
RYG
.
041
.
.
.
.I
.
.
-4
.
.
0
o 8
-0.1 1, -5
.
, I >’ -3 -2 -I Induced weight
I I 0 I change,
,A 2 kg
3
-01
I 4
(ABw-ABW,,,)
Fig. 1. Rates of weight change during a 3-week post-treatment period compared with hormone-induced weight changes in reindeer. Induced weight change of each animal is expressed as the difference between actual weight change and the mean change of control animals. *given physiological saline during treatment period, A-given prolactin, a-given thyroid hormones, m-given prolactin and triiodothyronine.
By the end of the treatment period, the rumens of animals given thyroxine were larger than those of t, controls, and this may have increased the capacity for
!overeating. The compensatory gain was more pronounced in this investigation than after weight loss induced by food restriction (Ryg & Jacobsen, 1982a). Qn the other hand, the turnover of thyroxine is increased by thyroxine treatment (Cullen et al., 1973), and in the present experiments, thyroxine turnover may have been faster than that reported by Yousef & .Luick (1971). Also, the relationship between weight changes and dry matter intake were similar in controls and hormone-treated animals during the posttswment period (Fig. 2), whereas during treatment, ‘#mals given thyroid hormones consumed more but ‘@ned lessthan controls (Ryg & Jacobsen, 19826).The biological halftime of prolactin is about f hr (Daughaday, 1974), making it less probable that the specific effects of this hormone extended much beyond the end of the treatment period. *The inverse relationships between compensatory .and induced weight changes suggest that during winter, the body weight of reindeer fed concentrate is iegulated with reference to a set-point, and that compensation i+ proportional to the deviation from that set-point. The :nature of such set-points are not known. It -probabJyinvolves monitoring of the sizeof fat depots; via the central nervous system (Panksepp, 1974).dr via .&repression of the gastrointestinal tract as the v@lnme ofabdominal fat increases(Campling, l970). Forbes ‘(1977)*developed a model for food intake of sheep., in, which stable body weight was reached ‘without. invoking a reference signal for body weight. However, the model included monitoring of energy requirements, which may be equivalent to a
kA
Dry ma&r
intak::
kg,:;
Fig. 2. Rates of weight change in relation to dry matter intake in the post-treatment period. Symbols as in Fig. 1.
functional set-point (Mrosovsky & Powley, 1977). Eriksson
et al. (1981) observed
that the feeding ac-
tivity of reindeer was mainly determined by the interaction between daylength and an ultradian behavioural rhythm. However, the amount of food taken during each bout of feeding was not recorded. Compensation could therefore be attained by differences in rates of consumption during each feeding period. Compensation may also have involved differences in energy expenditure, since animals previously treated with prolactin gained less weight, but did not eat significantly less than controls (Fig. 2). In contrast to the present results, Verme & Ozoga (1980) found that white-tailed fawns fed a low-energy diet in autumn gained less weight than those fed a high-energy diet, but did not compensate by increasing dry matter intake. The apparent disagreement between the findings of Verme & Ozoga on one hand, and those of Amman et al. (1973) and the present results, on the other, could be due to seasonal differences, since the first experiment was performed in autumn, and the other two in winter. Since the body weight of cervids fed a standard diet ad libitum rarely is constant, but either increases or decreases,one would have to postulate a seasonally variable set-point if the same mechanism regulates food intake throughout the year. Evidence for periodical lowering of the set-points for body weight in a number of vertebrates were reviewed by Mrosovsky & Sherry (1980). There is no evidence, however, suggesting that increased food intake in the summer season is due to a set-point elevation. In summary, it was found that compensatory weight changes occurred after hormone-induced weight changes in yearling reindeer. This is interpreted as evidence for involvement for a functional set-point in the regulation of food intake in reindeer.
Acknowledgements-This investigation was supported by the Norwegian Council for Science and the Humanities, by various grants from the University of Oslo, and by Tryggve Gotaas’ Foundation. I thank the staff at the Norwegian State Reindeer Research for help during the experiments.
Weight changes in reindeer REFERENCES
AMMAN A. P., COWAN R. L., MOTHERSHEAD GARDT B. R. (1973) Dry matter energy
C. L. & BAUM-
intake in relation
to digestibility in white-tailed deer. J. Wild/. Mgmt. 37, 1955201. BAILE C. A. & FORBES J. M. (1974) Control of feed intake and regulation of energy balance in ruminants. Physic/. Rev. 54, 160-213. CAMPLING R. C. (1970) Physical regulation of voluntary intake. In Physiology of digestion and Metabolism in the Ruminant (Edited bv PHILLIP~N A. T.). DD. 226234. Oriel Press, Newcasile-upon-Tyne. .. CULLEN M. J., DOHERTYG. F. & INGBAR S. H. (1973) The effect of hypothyroidism and thyrotoxicosis on thyroxine metabolism in the rat. Endocrinology 92, 1028-1033. DAUGHADAY W. H. (1978) The adenohypophysis. In Textbook of Endocrinology (Edited by WILLIAMS R. H.), pp. 31-79. W. B. Saunders Philadelphia. ERIKS~~N L.-O., K~~LLQVIST M.-L. & MOBBING T. (1981) Seasonal development of circadian and short-term activity in captive reindeer, Rangifer terandus L. Oecologia (Bed.) 48, M-70. FORBES J. M. (1977) Interrelationships between physical and metabolic control of voluntary food intake in fattening, pregnant and lactating mature sheep: A model. Anim. Prod. 24, 91-101. INGBAR S. H. & WOEBER
K. A. (1974) The thyroid gland. In
Textbook 01 Endocrinology (Edited by WILLIAMS, R: H.). pp. 955232. W. B. Saunders. Philadelphia. M~EWAN E. H. (1975) The adapt&, significance of the growth patterns in cervid compared with the other ungulate species. Zoo/. Zh. 54, 1221-1232. MRO~~VSKY N. & POWLEY T. L. (1977) Set points for body weight and fat. Eehar. Biol. 20, 2055223. MROSOVSKY N. & SHERRYD. F. (1980) Animal anorexias. Science,
Wash. 207, 837-842.
PANKSEPP J. (1974) Hvnothalamic regulation of enera! balance and feeding behaviour.- Fed. Pmt. 3?, 1150-1165. RYG M. & JACOBSEN E. (19820) Seasonal changes in growth rate, feed intake, growth hormone and thyroid hormones in young male reindeer (Rungifer tcrrandus tctrandus). Can. J. Zoo/.
60. 15-23.
RYG M. & JACOBSEN E. (1982b) Effects of thyroid hormones and prolactin on food intake and weight changes in young male reindeer (Rnngifer tcrrtmdus tarandus). Can. J. Zoo/.
60.
VERME L. J. & OZOGA J. J. (1980) Influence of proteinenergy intake on deer fawns in autumn. J. Wild/. Mgmt. 44. 305-314. YOUSEF M. K. & LUICK J. R. (1971) Estimation of thyroxine secretion rate in reindeer, Rungifrr tarandus: Effects of sex, age and season. Camp. Biochem. Physiol. 40A.789-795.
0300.9h29,;83i01033-03~3.00~0 0 1983 Pergnmon Press Ltd
RELATIONSHIPS BETWEEN HORMONE-INDUCED AND COMPENSATORY WEIGHT CHANGES IN REINDEER (RANGIFER TARANDUS TARANDUS) MORTEN
Institute
of
Zoophysiology,
RYG
University of Oslo, P.O. Box 1031 Blindern. Oslo 3, Norway (Received
30 March
1982)
Abstract-l. In connection with a study of hormonal effects on food consumption in reindeer, weight changes during treatment were compared with weight changes during a 3-week period following treatment. 2. Rates of weight change during the post-treatment period were inversely proportional to induced weight changes. 3. This inverse relationship is interpreted as evidence for a functional set-point for body weight in reindeer.
INTRODUCTION
Most models considering food intake are based on the assumptions of control of energy balance or maintenance of a stable body weight. However, in a number of species, including many northern ruminants, body weight is not stable, but oscillates between maximal levels in autumn and minima1 levels in spring (McEwan, 1975). This pattern is maintained also with free access to food, and raises the question of how food intake is regulated in these species. Eriksson et al. (198 1) suggested that food intake of reindeer is primarily regulated by the effect of daylength on an ultradian feeding rhythm, with little reference to physiological control. Also, Verme & Ozoga (1980) found that dry matter intake of white-tailed fawns in autumn was little affected by the energy content of the feed. In contrast, Amman et al. (1973) found that digestible energy intake of white-tailed deer fawns in winter was constant when a concentrate diet was progressively diluted with sawdust, as long as digestibility was above 50%. In the present paper, a set-point for body weight is considered as a possible control mechanism. Compensatory weight changes following periods of force-feeding or reduced food access is taken as evidence for a set-point, although the term is often used in a functional sense, and do not necessarily imply the existence of an actual reference signal (Mrosovsky & Powley, 1977). Although similar mechanisms have also been suggested for domestic ruminants (Baile & Forbes, 1974), studies involving fasting in ruminants is complicated by the large and variable gastrointestinal volume of these animals. In connection with an investigation of effects of thyroid hormones and prolactin on reindeer, posttreatment weight changes were compared with weight changes during treatment. Although opposite in their effects on weight gain, these hormones all caused increased food intake, thus probably excluding bias due to filling the rumen during the post-treatment period. If there is a defended body weight. one would expect
that the rate of weight change in the post-treatment period should be inversely related to the induced weight change. MATERIALS
AND
METHODS
The keeping of animals, and hormone treatment, has been described elsewhere (Ryg & Jacobsen, 1982a), Briefly, in three experiments, a total of 24 yearling reindeer bulls were treated with thyroid hormones Il.0 mg triiodothyronine (Sigma T-2877) or 1.2 mg triiodothyronine and 2.4 mg thyroxine (Sigma T-2376) per day], or prolactin [I70 or 250 i.u. ovine prolactin (Sigma L-4876) per day] for 2-4 weeks. The animals were fed a pelleted reindeer feed (RF 71) containing 13.7% protein. 7.2% fat, 62.4% nitrogen-free extracts, 11% crude fiber, and 5.7% ash. Food intake and body weight was recorded during the hormone treatment and a following 3-week period. RESULTS
During the post-treatment period, individual rates of weight change were negatively correlated (r = 0.83, P < 0.01) with the weight changes during the treatment period (Fig. 1). The induced weight change of each animal is expressed as the difference between total weight change in the treatment period and the mean change of the control animals in each experiment. Weight changes in the post-treatment period were significantly correlated with dry matter intake (r = 0.76, P < 0.01) (Fig. 2). For a given dry matter intake, weight gain in animals previously treated with prolactin tended to be lower than in controls. DISCUSSION
Residual effects of the hormone treatment could possibly explain some of the differences in the posttreatment period, especially in animals treated with thyroid hormones. The biological halftime of triiodothyronine in humans is about 1 day (Ingbar & Woeber, 1974) and in yearling reindeer, the halftime of thyroxine is about 3 days (Yousef & Luick, 1971).
MORTEN
RYG
.
041
.
.
.
.I
.
.
-4
.
.
0
o 8
-0.1 1, -5
.
, I >’ -3 -2 -I Induced weight
I I 0 I change,
,A 2 kg
3
-01
I 4
(ABw-ABW,,,)
Fig. 1. Rates of weight change during a 3-week post-treatment period compared with hormone-induced weight changes in reindeer. Induced weight change of each animal is expressed as the difference between actual weight change and the mean change of control animals. *given physiological saline during treatment period, A-given prolactin, a-given thyroid hormones, m-given prolactin and triiodothyronine.
By the end of the treatment period, the rumens of animals given thyroxine were larger than those of t, controls, and this may have increased the capacity for
!overeating. The compensatory gain was more pronounced in this investigation than after weight loss induced by food restriction (Ryg & Jacobsen, 1982a). Qn the other hand, the turnover of thyroxine is increased by thyroxine treatment (Cullen et al., 1973), and in the present experiments, thyroxine turnover may have been faster than that reported by Yousef & .Luick (1971). Also, the relationship between weight changes and dry matter intake were similar in controls and hormone-treated animals during the posttswment period (Fig. 2), whereas during treatment, ‘#mals given thyroid hormones consumed more but ‘@ned lessthan controls (Ryg & Jacobsen, 19826).The biological halftime of prolactin is about f hr (Daughaday, 1974), making it less probable that the specific effects of this hormone extended much beyond the end of the treatment period. *The inverse relationships between compensatory .and induced weight changes suggest that during winter, the body weight of reindeer fed concentrate is iegulated with reference to a set-point, and that compensation i+ proportional to the deviation from that set-point. The :nature of such set-points are not known. It -probabJyinvolves monitoring of the sizeof fat depots; via the central nervous system (Panksepp, 1974).dr via .&repression of the gastrointestinal tract as the v@lnme ofabdominal fat increases(Campling, l970). Forbes ‘(1977)*developed a model for food intake of sheep., in, which stable body weight was reached ‘without. invoking a reference signal for body weight. However, the model included monitoring of energy requirements, which may be equivalent to a
kA
Dry ma&r
intak::
kg,:;
Fig. 2. Rates of weight change in relation to dry matter intake in the post-treatment period. Symbols as in Fig. 1.
functional set-point (Mrosovsky & Powley, 1977). Eriksson
et al. (1981) observed
that the feeding ac-
tivity of reindeer was mainly determined by the interaction between daylength and an ultradian behavioural rhythm. However, the amount of food taken during each bout of feeding was not recorded. Compensation could therefore be attained by differences in rates of consumption during each feeding period. Compensation may also have involved differences in energy expenditure, since animals previously treated with prolactin gained less weight, but did not eat significantly less than controls (Fig. 2). In contrast to the present results, Verme & Ozoga (1980) found that white-tailed fawns fed a low-energy diet in autumn gained less weight than those fed a high-energy diet, but did not compensate by increasing dry matter intake. The apparent disagreement between the findings of Verme & Ozoga on one hand, and those of Amman et al. (1973) and the present results, on the other, could be due to seasonal differences, since the first experiment was performed in autumn, and the other two in winter. Since the body weight of cervids fed a standard diet ad libitum rarely is constant, but either increases or decreases,one would have to postulate a seasonally variable set-point if the same mechanism regulates food intake throughout the year. Evidence for periodical lowering of the set-points for body weight in a number of vertebrates were reviewed by Mrosovsky & Sherry (1980). There is no evidence, however, suggesting that increased food intake in the summer season is due to a set-point elevation. In summary, it was found that compensatory weight changes occurred after hormone-induced weight changes in yearling reindeer. This is interpreted as evidence for involvement for a functional set-point in the regulation of food intake in reindeer.
Acknowledgements-This investigation was supported by the Norwegian Council for Science and the Humanities, by various grants from the University of Oslo, and by Tryggve Gotaas’ Foundation. I thank the staff at the Norwegian State Reindeer Research for help during the experiments.
Weight changes in reindeer REFERENCES
AMMAN A. P., COWAN R. L., MOTHERSHEAD GARDT B. R. (1973) Dry matter energy
C. L. & BAUM-
intake in relation
to digestibility in white-tailed deer. J. Wild/. Mgmt. 37, 1955201. BAILE C. A. & FORBES J. M. (1974) Control of feed intake and regulation of energy balance in ruminants. Physic/. Rev. 54, 160-213. CAMPLING R. C. (1970) Physical regulation of voluntary intake. In Physiology of digestion and Metabolism in the Ruminant (Edited bv PHILLIP~N A. T.). DD. 226234. Oriel Press, Newcasile-upon-Tyne. .. CULLEN M. J., DOHERTYG. F. & INGBAR S. H. (1973) The effect of hypothyroidism and thyrotoxicosis on thyroxine metabolism in the rat. Endocrinology 92, 1028-1033. DAUGHADAY W. H. (1978) The adenohypophysis. In Textbook of Endocrinology (Edited by WILLIAMS R. H.), pp. 31-79. W. B. Saunders Philadelphia. ERIKS~~N L.-O., K~~LLQVIST M.-L. & MOBBING T. (1981) Seasonal development of circadian and short-term activity in captive reindeer, Rangifer terandus L. Oecologia (Bed.) 48, M-70. FORBES J. M. (1977) Interrelationships between physical and metabolic control of voluntary food intake in fattening, pregnant and lactating mature sheep: A model. Anim. Prod. 24, 91-101. INGBAR S. H. & WOEBER
K. A. (1974) The thyroid gland. In
Textbook 01 Endocrinology (Edited by WILLIAMS, R: H.). pp. 955232. W. B. Saunders. Philadelphia. M~EWAN E. H. (1975) The adapt&, significance of the growth patterns in cervid compared with the other ungulate species. Zoo/. Zh. 54, 1221-1232. MRO~~VSKY N. & POWLEY T. L. (1977) Set points for body weight and fat. Eehar. Biol. 20, 2055223. MROSOVSKY N. & SHERRYD. F. (1980) Animal anorexias. Science,
Wash. 207, 837-842.
PANKSEPP J. (1974) Hvnothalamic regulation of enera! balance and feeding behaviour.- Fed. Pmt. 3?, 1150-1165. RYG M. & JACOBSEN E. (19820) Seasonal changes in growth rate, feed intake, growth hormone and thyroid hormones in young male reindeer (Rungifer tcrrandus tctrandus). Can. J. Zoo/.
60. 15-23.
RYG M. & JACOBSEN E. (1982b) Effects of thyroid hormones and prolactin on food intake and weight changes in young male reindeer (Rnngifer tcrrtmdus tarandus). Can. J. Zoo/.
60.
VERME L. J. & OZOGA J. J. (1980) Influence of proteinenergy intake on deer fawns in autumn. J. Wild/. Mgmt. 44. 305-314. YOUSEF M. K. & LUICK J. R. (1971) Estimation of thyroxine secretion rate in reindeer, Rungifrr tarandus: Effects of sex, age and season. Camp. Biochem. Physiol. 40A.789-795.