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The rôles of photoperiod and nutrition in the seasonal increases in growth and insulin-like growth factor-1 secretion in male red deer

Published online by Cambridge University Press:  18 August 2016

J. R. Webster ,
I. D. Corson ,
R. P. Littlejohn ,
S. K. Martin  and
J. M. Suttie
J. R. Webster*
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
I. D. Corson
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
R. P. Littlejohn
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
S. K. Martin
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
J. M. Suttie
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
*
†E-mail:jim.webster@agresearch.co.nz
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Abstract

Young male red deer follow a seasonal growth pattern that can be shifted by altering the photoperiod they experience. An increase in photoperiod to 16 h of light per day (16L : 8D) during winter advances the onset of rapid growth and high food intake that normally commences in spring. These changes are associated with increased growth hormone (GH) and insulin-like growth factor-1 (IGF-1) secretion. The GH/IGF-1 axis is acutely sensitive to the level of nutrition and the relative rôles of photoperiod and nutrition in determining the spring IGF-1 rise is unknown. The present experiment set out to examine this by exposing two groups of deer (no. = 8 per group) to a photoperiod shift during their 1st year of life (16L : 8D from 2 June), designed to cause accelerated growth and increased food intake after approximately 7 weeks. However, after 6 weeks the food intake (pellets containing 11 MJ metabolizable energy and 160 g crude protein per kg dry matter (DM)) of one group (LDRES) was clamped, thereby preventing the intake component of the response. The intake of the other group (LDAL) remained ad libitum for a further 12 weeks until 6 October, when the experiment concluded.

During the first 6 weeks of 16L : 8D, growth rate (118 (s.e. 15·4) g/day) and food intake (1·37 (s.e. 0·031) kg DM per head per day) did not differ between the groups. Food intake following the clamp in LDRES averaged 1·40 (s.e. 0·015) kg per head per day. The intake of LDAL increased 2 weeks after the clamp and thereafter was higher than LDRES (P < 0·001). Food intake of LDAL averaged 2·13 (s.e. 0·051) kg during the nutritional clamp period. Growth rates increased in both groups during the first 3 weeks of the clamp, averaging 237 (s.e. 25·0) g/day, then growth slowed in LDRES and live weights diverged. Growth rates until the end of the experiment (147 (s.e.23·0) g/ day v. 299 (s.e. 12·5) g/day, P < 0·001) and mean live weight over the last 5 weeks of the experiment were lower (P < 0·05) in LDRES than LDAL, weights reaching 88·3 (s.e. 1·86) kg and 97·9 (s.e. 2·74) kg respectively on the final sampling date. Metatarsal bone length grew more in LDAL than in LDRES (3·1 v. 2·2 cm, s.e.d. = 0·23, P < 0·01). Prior to the nutritional clamp, mean plasma prolactin and IGF-1 concentrations increased at 3 and 6 weeks after 16L : 8D respectively, in both groups. Prolactin concentrations were lower in LDRES than LDAL on two occasions, at weeks 3 and 7 after the onset of the nutritional clamp, and IGF-1 concentrations were lower in LDRES than LDAL (676 v. 872 ng/ml, s.e.d. = 73·8, P < 0·05) over the last 7 weeks of sampling.

In summary, a photoperiodically driven increase in IGF-1 occurred even when the usual associated increase in food intake was prevented. This indicates that the seasonal IGF-1 rise in red deer is not a consequence of the increased food intake, although the latter appears necessary to maintain elevated IGF-1 concentrations. The rise in IGF-1 may therefore be considered as a component of the photoperiodically entrained seasonal drive to grow, and the increase in food intake a response to satisfy the increased energy demand.

Keywords

nutritionphotoperiodred deer
Type
Non-ruminant, nutrition, behaviour and production
Information
Animal Science , Volume 73 , Issue 2 , October 2001 , pp. 305 - 311
Copyright
Copyright © British Society of Animal Science 2001

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References

Adam, C. L., Kyle, C. E. and Young, P. 1996. Seasonal patterns of growth, voluntary food intake and plasma concentrations of prolactin, insulin-like growth factor-1, LH and gonadal steroids in male and female pre-pubertal red deer (Cervus elaphus) reared in either natural photoperiod or constant daylength. Animal Science 62: 605–613.Google Scholar
Adam, C. L., Kyle, C. E., Young, P. and Atkinson, T. 1995. Effect of nutritional growth restriction on timing of reproductive development and plasma concentrations of insulin-like growth factor-1 and growth hormone in male red deer (Cervus elaphus) reared in constant photoperiod. Animal Science 61: 155–160.CrossRefGoogle Scholar
Arendt, J. and Marks, V. 1982. Physiological changes underlying jet lag. British Medical Journal 284: 144–146.Google Scholar
Asher, G. W., Muir, P. D., Semiadi, G., O’Neill, K.T., Scott, I. C. and Barry, T. N. 1997. Seasonal patterns of luteal cyclicity in young red deer (Cervus elaphus) and sambar deer (Cervus unicolor). Reproduction, Fertility and Development 9: 587–596.CrossRefGoogle Scholar
Baker, J. R. 1938. The evolution of breeding seasons. In Evolution: essays on aspects of evolutionary biology, presented to Professor Goodrich, E. F. on his seventieth birthday (ed. Beer, G. R. de), pp. 161–177. Clarendon, Oxford.Google Scholar
Barrell, G. K., Muir, P. D. and Sykes, A. R. 1985. Seasonal profiles of plasma testosterone, prolactin, and GH in red deer stags. In Biology of deer production (ed. Fennessy, P. F. and Drew, K. R.), Proceedings of the Royal Society of New Zealand, vol. 22, pp. 185–190.Google Scholar
Blaxter, K. L., Kay, R. N. B., Sharman, G. A. M., Cunningham, J. M. M. and Hamilton, W. J. 1974. Farming the red deer. The first report of an investigation by the Rowett Research Institute and the Hill Farming Research Organisation. Her Majesty’s Stationery Office, Edinburgh.Google Scholar
Brinklow, B. R. and Loudon, A. S. I. 1990. The role of photoperiod in the postnatal development of seasonal rhythms in deer. Journal of Interdisciplinary Cycle Research 21: 173–175.Google Scholar
Brown, W. B., Forbes, J. M., Goodall, E. D., Kay, R. N. B. and Simpson, A. M. 1979. Effects of photoperiod on food intake, sexual condition and hormone concentrations in stags and rams. Journal of Physiology 296: 58P–59P.Google ScholarPubMed
Clutton-Brock, T.H, Guinness, F. E. and Albon, S.D. 1982. Red deer: behaviour and ecology of two sexes. University of Chicago Press, Chicago.Google Scholar
Cohick, W. S., Vicini, J. L., Staples, C. R., Clark, J. H., McCutcheon, S. N. and Bauman, D. E. 1986. Effects of intake and postruminal casein infusion on performance and concentrations of hormones in plasma of lactating cows. Journal of Dairy Science 69: 3022–3031.Google Scholar
Curlewis, J. D., Loudon, A. S. I., Milne, J. A. and McNeilly, A. S. 1988. Effects of chronic long-acting bromocriptine treatment on liveweight, voluntary food intake, coat growth and breeding season in non-pregnant red deer hinds. Journal of Endocrinology 119: 413–420.Google Scholar
Drew, K. R. 1976. The farming of red deer in New Zealand. World Review of Animal Production 12: 49–60.Google Scholar
Fennessy, P. F. 1982. Growth and nutrition. In The farming of deer. World trends and modern techniques (ed. Yerex, D.), pp. 105–114. Agricultural Promotion Associates Ltd, Wellington, New Zealand.Google Scholar
Foster, D. L., Ebling, F. J. P., Micka, A. F., Vannerson, L. A., Bucholtz, D. C., Wood, R. I., Suttie, J. M. and Fenner, D. E. 1989. Metabolic interfaces between growth and reproduction. 1. Nutritional modulation of gonadotropin, prolactin, and growth hormone secretion in the growth-limited female lamb. Endocrinology 125: 342–350.CrossRefGoogle ScholarPubMed
Gluckman, P. D., Douglas, R. G., Ambler, G. R., Breier, B. H., Hodgkinson, S. C., Koea, J. B. and Shaw, J. H. F. 1991. The endocrine role of insulin-like growth factor I. Acta Paediatrica Scandinavia 372: 97–105.Google Scholar
Gorman, M. R., Freeman, D. A. and Zucker, I. 1997. Photoperiodism in hamsters: abrupt versus gradual changes in day length differentially entrain morning and evening circadian oscillators. Journal of Biological Rhythms 12: 122–135.CrossRefGoogle ScholarPubMed
Hua, K. M., Ord, R., Kirk, S., Li, Q. J., Hodgkinson, S. C., Spencer, G. S. G., Molan, P. C. and Bass, J. J. 1993. Regulation of plasma and tissue levels of insulin-like growth factor-I by nutrition and treatment with growth hormone in sheep. Journal of Endocrinology 136: 217–224.Google Scholar
Hunter, W. M. and Greenwood, F. C. 1962. Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature 194: 495–496.Google Scholar
Kay, R. N. B. 1988. Seasonal variation of appetite in ruminants. In Recent developments in ruminant nutrition 2 (ed. W. Haresign and D. Cole, J. A.), pp. 34–45. Butterworths, London.Google Scholar
Kenward, M. G. 1987. A method for comparing profiles of repeated measurements. Applied Statistics 36: 296–308.Google Scholar
Lincoln, G. A. 1998. Photoperiod-melatonin relay in deer. Acta Veterinaria Hungarica 46: 341–356.Google Scholar
Loudon, A. S. I. 1994. Photoperiod and the regulation of annual and circannual cycles of food intake. Proceedings of the Nutrition Society 53: 495–507.CrossRefGoogle ScholarPubMed
Monk, T. H., Moline, M. L. and Graeber, R. C. 1988. Inducing jet lag in the laboratory: patterns of adjustment to an acute shift in routine. Aviation, Space and Enviromental Medicine 59: 703–710.Google Scholar
Moore, L. G. and Mylek, M. E. 1993. A novel method for the extraction of sheep insulin-like growth factors-I and -II from plasma prior to radioimmunoassay. Journal of Endocrinology 137: 239–245.CrossRefGoogle ScholarPubMed
Robinson, J. E., Wayne, N. L. and Karsch, F. J. 1985. Refractoriness to inhibitory day lengths initiates the breeding season of the Suffolk ewe. Biology of Reproduction 32: 1024–1030.Google Scholar
Ryg, M. and Jacobsen, E. 1982. Effects of thyroid hormones and prolactin on food intake and weight changes in young male reindeer (Rangifer tarandus tarandus). Canadian Journal of Zoology 60: 1562–1567.Google Scholar
Simpson, A. M., Suttie, J. M. and Kay, R. N. B. 1983/84. The influence of artificial photoperiod on the growth, appetite and reproductive status of male red deer and sheep. Animal Reproduction Science 6: 291–299.Google Scholar
Suttie, J. M. and Corson, I. D. 1991. Deer growth and production: a review. Proceedings of the Deer Branch of the New Zealand Veterinary Association 8: 53–67.Google Scholar
Suttie, J. M., Corson, I. D., Gluckman, P. D. and Fennessy, P. F. 1991a. Insulin-like growth factor 1, growth and body composition in red deer stags. Animal Production 53: 237–242.Google Scholar
Suttie, J. M., Fennessy, P. F., Corson, I. D., Laas, F. J., Crosbie, S. F., Butler, J. H. and Gluckman, P. D. 1989. Pulsatile growth hormone, insulin-like growth factors and antler development in red deer (Cervus elaphus scoticus) stags. Journal of Endocrinology 121: 351–360.CrossRefGoogle Scholar
Suttie, J. M., Goodall, E. D., Pennie, K. and Kay, R. N. B. 1983. Winter food restriction and summer compensation in red deer stags (Cervus elaphus). British Journal of Nutrition 50: 737–747.Google Scholar
Suttie, J. M. and Simpson, A. M. 1985. Photoperiodic control of appetite, growth, antlers and endocrine status of red deer. In Biology of deer production (ed. Fennessy, P. F. and Drew, K. R.), Proceedings of the Royal Society of New Zealand, vol. 22, pp. 429–432.Google Scholar
Suttie, J. M. and Webster, J. R. 1995a. Are arctic ungulates physiologically unique? Rangifer 18: 99–118.Google Scholar
Suttie, J. M. and Webster, J. R. 1995b. Extreme seasonal growth in arctic deer: comparisons and control mechanisms. American Zoologist 35: 215–221.Google Scholar
Suttie, J. M., Wenham, G. and Kay, R. N. B. 1984. Influence of winter feed restriction and summer compensation on skeletal development in red deer stags (Cervus elaphus). Research in Veterinary Science 36: 183–186.CrossRefGoogle ScholarPubMed
Suttie, J. M., White, R. G., Breier, B. H. and Gluckman, P. D. 1991b. Photoperiod associated changes in insulin-like growth factor-I in reindeer. Endocrinology 129: 679–682.Google Scholar
Tapp, W. N. and Natelson, B. H. 1989. Circadian rhythms and patterns of performance before and after simulated jet lag. American Journal of Physiology 257: R796–803.Google Scholar
Webster, J. R., Corson, I. D., Littlejohn, R. P., Masters, B. M. and Suttie, J. M. 2000. Effect of diet energy density and season on voluntary dry-matter and energy intake in male red deer. Animal Science 70: 547–554.CrossRefGoogle Scholar
Webster, J. R., Corson, I. D., Littlejohn, R. P., Stuart, S. K. and Suttie, J. M. 1996. Effects of season and nutrition on growth hormone and insulin-like growth factor-I in male red deer. Endocrinology 137: 698–704.Google Scholar
Webster, J. R., Corson, I. D., Littlejohn, R. P., Stuart, S. K. and Suttie, J. M. 1998. Photoperiodic requirements for rapid growth in young male red deer. Animal Science 67: 363–370.Google Scholar
Webster, J. R., Corson, I. D., Littlejohn, R. P., Stuart, S. K. and Suttie, J. M. 1999. Effects of photoperiod on the cessation of growth during autumn in male red deer and growth hormone and insulin-like growth factor-I secretion. General and Comparative Endocrinology 113: 464–477.Google Scholar
Woodfill, C. J. I., Robinson, J. E., Malpaux, B. and Karsch, F. J. 1991. Synchronization of the circannual reproductive rhythm of the ewe by discrete photoperiodic signals. Biology of Reproduction 45: 110–121.Google Scholar