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

Abstract

AbstractYoung 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.