Extreme Seasonal Growth in Arctic Deer: Comparisons and Control Mechanisms 1

Transcription

1 AMER. ZOOL., 35: (1995) Extreme Seasonal Growth in Arctic Deer: Comparisons and Control Mechanisms 1 JAMES M. SUTTIE AND JAMES R. WEBSTER AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand SYNOPSIS. Arctic ungulates have the capacity to voluntarily restrict growth to times of the year of predictable high quality seasonal herbage abundance. The constraints of the arctic environment mean that not only must the timing of this growth seasonality be accurate but growth rate must be maximised for a short period of time. It is known that daylength is a critical cue for the timing of seasonal rhythms of growth; a manipulated photoperiod of 16L:8D stimulates out of season growth in reindeer during winter and this growth is associated with an increase in the plasma levels of insulin like growth factor 1 (IGF 1). In contrast a manipulated photoperiod of 8L: 16D delays the spring rise in growth. There is good evidence from a boreal cervid, the red deer, that the number of hours of day influences growth rate also and this is associated with IGF 1. Thus daylength may have a dual role in growth seasonality, timing and amplitude. Although the mechanisms underlying the timing of rhythms by daylength are partly understood a putative role for daylength in controlling the rate of an event is a new concept. INTRODUCTION The extreme fluctuations in annual temperature, daylength and herbage growth make the Arctic regions some of the most seasonal environments on earth. During summer, when daylight is continuous the forage quality of tundra plants is very high but this period is very short (Klein, 1970). Ungulates have adapted to these extreme conditions in a number of ways (Sadleir, 1969); breeding seasons are brief and precisely timed so that calving is concentrated to the optimal period for offspring survival (Dauphine and McClure, 1974), caribou (Rangifer tarandus) herds may be highly migratory (Klein, 1970) and growth is largely restricted to the periods of summer food abundance (McEwan, 1968). The aim of this paper is firstly to review the phenomena of seasonal growth in various species of deer but with reference particularly to Arctic deer and secondly, propose a control mechanism for the extreme seasonal growth pattern observed in Arctic deer. 1 From the Symposium Endocrinology of Arctic Birds and Mammals presented at the Annual Meeting of the American Society of Zoologists, December 1993, at Los Angeles, California. Seasonal Growth Increased liveweight gain during summer in comparison to winter has been recorded in all arctic, boreal and temperate deer so far studied, white-tailed deer (Odocoileus virginianus) (French, et ai, 1956), mule deer (O. hemionus) (Bandy et al, 1970), caribou (McEwan and Whitehead, 1966; McEwan, 1968), reindeer (R. tarandus) (Ryg and Jacobsen, 1982), moose {Alces alces), (Franzmann et al., 1978), roe deer {Capreolus capreolus), (Drozdz et al., 1975), fallow deer (Dama dama) (Asher, 1993), red deer (Cervus elaphus) (Pollock, 1975; Simpson, et al., 1983) and wapiti (C. elaphus) (Haigh and Hudson 1992). In contrast, data from tropical deer point either to reduced seasonality of growth or aseasonality (Suttie et al., 1993). In experimental studies, in which deer have been fed high quality rations to appetite throughout the year, it has been shown that the cycle of liveweight persists and that the deer voluntarily reduce their appetite during winter (McEwan, 1968; Suttie et al., 1983). The cycle of voluntary food intake and growth are known to be under photoperiodic control (Suttie and Simpson, 1985). Whereas for reproductive seasonality the short days of autumn are thought to 215

2 216 J. M. SUTTIE AND J. R. WEBSTER i 1 1 i i i i Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sept Month FIG. 1. The cumulative % of maximum yearling male liveweight achieved each month in three species of deer. (Reindeer data, Ryg and Jacobsen, 1982; Red deer, Suttie and Fennessy, unpublished; Rusa deer, Suttie and Woodford, unpublished). provide a stimulatory cue for reproduction in temperate deer, it appears the long days of spring provide a stimulatory cue for increased food intake and hence growth. In a species living in a seasonal environment the penalty for breeding at a sub optimal time is poor or zero survival of offspring. This in turn leads to a genetic control of breeding seasons where mating is timed so that young are born at the time of year best suited to survival. There is strong evidence from rabbits and deer that the timing of mating and hence parturition is more concentrated in time with increasing latitude (Sadleir, 1969). Clearly, the penalties of breeding too early or too late are more Severe in Arctic climates. In the same way in a seasonal environment the onset of rapid herbage growth is largely predictable from year to year (indeed this is the event parturition is timed to coincide with) and this may have some consequences for deer growth. The fact that the calving is concentrated in Arctic ungulates might be due to predation but the timing of the concentrated period of calving is probably in response to nutritional factors. It is assumed that in red deer there are strong selection pressures particularly for males to grow as large as possible to increase reproductive success (Clutton-Brock et at, 1983). Arctic deer are also relatively large and it is likely that they must attain a certain surface area/volume ratio for energy conservation. Arctic deer have a very strong selection pressure to grow large but if they attempted to alter their metabolism to increase growth in the absence of available food then death could result. On the contrary, if they delayed the onset of growth until forage was available the opportunity could be lost while they adjusted to the conditions. If plant growth is highly seasonal then animals must have the ability to grow rapidly for a short period of time to take advantage of the seasonal abundance. In the same way that they use photoperiod to time the breeding season, it is proposed that they also use photoperiod to accurately time the growing season to anticipate the seasonal bounty of feed. It would thus be predicted that Arctic species of deer would delay the onset of seasonal growth, but grow more rapidly relative to species of deer from temperate or tropical climates. To test this, data were examined from male rusa deer, red deer and reindeer from tropical temperate and arctic climates, respectively (Fig. 1). Deer had been fed to appetite on high quality diets from birth to 15 mo of age. The data on the x-axis has been adjusted to account for the different birth seasons of the species and the location of the studies (Southern vs. Northern hemispheres). The percentage of the maximum yearling weight achieved each month was calculated and plotted against time. This revealed that yearling male rusa deer grow almost linearly but in contrast both red and reindeer have slower growth in winter than spring and summer. In addition, red deer began the summer period of rapid growth earlier than reindeer, but the reindeer appeared to grow more rapidly during a shorter summer period. It was decided to investigate the comparative relationships between deer species and growth rate/seasonality further. The concepts which were investigated are as follows a) As latitude increases does a greater proportion of growth take place in summer? b) Does photoperiod time the growth increase? c) Is it the absolute photoperiod (latitude

3 CONTROL OF SEASONAL GROWTH IN ARCTIC DEER 217 dependent), which increases the rate of growth via IGF 1? The evaluation of the data do not consider or adjust for pre-weaning nutrition. This was not measured in any study and in view of the data to come does not appear to be important. Comparative seasonal growth does more growth take place in summer at high latitudes? Body size data from wild populations are difficult to analyse because of nutritional, age, genotypic, year to year variation and because sample sizes often vary. Fortunately experimental studies under controlled conditions have been carried out on a number of deer species. Although it might be more relevant ecologically to analyse data from mature females, most of the available data is from yearling males. Yearling males are more seasonal than females and they have a high pressure to grow rapidly to enter the breeding population as early as possible. Consequently, the analysis was carried out exclusively on data from male deer in their first 14 mo of life. Data were obtained from published and unpublished sources (Table 1). For each case, the published value for weight gain during the 4 months of shortest daylength (W), the 4 months of longest daylength (S) and the maximum yearling liveweight (T) was recorded. From these data, the ratio of winter to summer growth (W/S) and the percentage of growth occurring in winter ( /o W) and summer (% S) was calculated. The latitude where the study took place and the latitude of origin of the deer (if different) was also noted. Latitude of origin was denned as different if the deer had been removed immediately before the study from their latitude of origin to the latitude of study. The W/S growth ratio varied greatly among the data sets, from for moose to 0.81 for rusa deer (Fig. 2). Overall, there was a trend that boreal/arctic species had lower ratios than species from lower latitudes. There was also a relationship between the proportion of growth in winter and the proportion of growth in summer such that deer which grew little in winter grew most fei a par 5 8 -e c "i a ILE 1. 2 H litude udy) 3S. tude gin) Lali (ori eight 3E -i maxi c ^ % total 1 summ 6 immer L c/> S E 'sum Wint 6 S c S I si 25 s c S S a: pecics >ooooooo IOOOOOOOOOOO 8 I s -' ' (N d od N<NN(N ooooooooooooooo ooooooooooooooo OO oo 2l«>- &J 3 a. c jo ooos a o caoaa_o> : v S «Ii ii g _ a u li o E S E 15

4 218 J. M. SUTTIE AND J. R. WEBSTER 40-, Species of deer and location study FIG. 2. The ratio of growth taking place in winter/ summer in deer of various species. See Table 1 for data references. 40-i 3 5, 35-1 in summer (Fig. 3). Arctic species of deer are near one extreme of this relationship and clearly grow most in summer. It must be re-emphasized that food was not limiting in any of the studies reported so these strong relationships between seasonality and growth are independent of food availability. Clearly, Arctic deer do not use highly abundant feed in winter; it is concluded that Arctic deer have an adaptive strategy to limit growth to periods of predictable food abundance. It is interesting to consider the mechanisms which underlay this pattern. Clearly, food availability is not a control mechanism. It is possible that environmental con J Proportion of annual growth in winter (%) FIG. 3. The proportion of growth in summer and the proportion of growth in winter in deer species J Hours of daylight 60 days from the summer solstice FIG. 4. Proportion of annual growth in summer and the hours of daylight 60 days prior to the summer solstice. ditions could influence growth because cold, by increasing maintenance requirements, could limit the supply of nutrients available for production. However, deer recently translocated to a different latitude resemble more closely the % S of their latitude of origin. A good example of this is the caribou caught in the wild as calves and translocated for the study which has a % S of 31% but other species at the latitude of study (Vancouver) have % S of 24%. In contrast red deer which have been in Queensland for 140 years have a % S more closely resembling the rasa deer than deer in the country of origin, UK. This suggests that latitude of origin may play a role in determining relative growth pattern. If % S and % W are plotted against the daylength at midsummer of the latitude of origin, there is a strong positive regression with summer growth rate and a strong negative regression with winter growth. It is at higher latitudes that deer grow faster in summer than in winter. In the sub-tropics (Australia) growth rate is similar in summer and winter. Indeed the relationship is stronger if it is calculated between daylength 60 days prior to the summer solstice and summer liveweight gain. The regression is y = 6.56 x where y = summer liveweight gain and x is the daylength in hours 60 days before the summer solstice. The correlation coefficient r = with a residual standard deviation of The significance of calculating the

5 CONTROL OF SEASONAL GROWTH IN ARCTIC DEER f If S~ J I LSD I LSD 16L:8D 16L:8D 8L:16D Time (weeks) FIG. 5. Liveweight and plasma IGF 1 in groups of reindeer calves exposed to 16L:8D or 8L: 16D from the autumnal to the spring equinox. daylength of 60 days before the summer solstice is that this was the onset of the period of summer growth as denned in the study. Higher latitudes are associated with long winter darkness and also long periods of daylight during summer. Typically daylength is thought of as the cue which accurately times the onset of seasonal events at least in arctic and temperate latitudes. The mechanism of action of daylength on growth rhythms is not known but the possibility arises that daylength could time the onset of spring growth. The fact that daylength is long during the Arctic summer introduces two other possibilities, namely that long daylength could stimulate rapid growth rate in summer and short daylength actually suppress growth during winter. Does photoperiod time the growth increase? To test whether Arctic deer responded to photoperiod for growth, a study was carried out on five month old male reindeer calves (Suttie et al., 1991). On the autumnal equinox one group of reindeer was exposed to 16 hr of light followed by 8 hr of dark (16L: 8D) and a second was exposed to 8L:16D. The animals were fed ad libitum in individual pens and were weighed and a blood sample taken every two weeks for six months. The group exposed to 16L:8D but not that exposed to 8L:16D began rapid growth after exposure to the photoperiod (Fig. 5). About six weeks after exposure to > to ' J 16:8 O :16 A Outside i 1 i Week of experiment 30 i 36 FIG. 6. Liveweight of red deer stags exposed to one of four manipulated daylengths or maintained outside as control. 16L:8D, plasma levels of insulin like growth factor 1 (IGF 1) increased also. In view of the fact that IGF 1 is known to mediate some of the anabolic effects of growth hormone (Salmon and Daughaday, 1957; Suttie et al., 1989), it was concluded that the elevation in growth rate was possibly a consequence of the IGF 1. This meant that not only was IGF 1 elevated due to a daylength manipulation but it could be associated with a biological effect, namely an increase in growth. It can be concluded in Arctic deer that daylength, acting via IGF 1, can act as a cue to time the onset of rapid growth. Could the photoperiodic effect on rate act via IGF 1? But what of an effect on growth rate? A study of red deer permitted the testing of an hypothesis that absolute daylength could influence not only the timing of growth but also rate by acting through IGF 1. Five groups of red deer stags aged seven months, (n = 10/group), were randomly allocated to daylength treatments which began on the winter solstice as follows: 16L: 8D, 13.25L:10.75D, 10.75L:13.25D, 8L: 16D, (all kept indoors) or control outside. All stags, including those outside, were fed ad libitum a concentrate ration only. The outside stags had no access to pasture. The study continued for 36 weeks and during that time the stags were weighed weekly and

6 220 J. M. SUTTEE AND J. R. WEBSTER f g soo x x mini I I I I I I I I I I I I i Time (weeks) A 16L8D 13 25L10 75D D 10 75LM3 25D O 8UI6D Outside FIG. 7. IGF 1 in red deer stags kept exposed to one of four manipulated daylengths or maintained outside as a control. blood samples were taken 1-2 weekly. All samples were analysed for IGF 1. The liveweight data are shown in Figure 6. Within six weeks of the treatment onset, the 16L:8D stags grew faster than all other groups. Growth of all the indoor groups conspicuously slowed 24 wk after the start of the study. This meant that the 13.25L: 10.75D, 10.75L:13.25D and 8L:16D groups were smaller than both the 16L:8D and outside control groups. In contrast, the outside control group grew at a steady rate throughout the study and indeed at the close were marginally heavier than the 16L:8D group. The outside control group showed the expected seasonal pattern of elevated IGF 1 during the mid part of the study which was during the summer (Fig. 7). However, the daylength treatments had different effects on IGF 1. Overall the 16L:8D group showed significantly elevated levels of IGF 1 four weeks after the study began and levels remained elevated throughout the experimental period. This group showed the strongest growth response. In contrast the 13.25L:10.75D group had elevated IGF 1 levels but did not show the increase in growth. Neither the 10.75L:13.25D group nor the 8L: 16D group had elevated IGF 1 levels during the first 16 weeks of the study compared with the outside control and both these groups had significantly lower peak (summer) IGF 1 compared to the outside control. These data indicate that absolute daylength influences not only the pattern of IGF 1 secretion but also the amount. Further, only the group (16L:8D) with consistently elevated IGF 1 showed the most rapid growth. It is tentatively proposed that seasonal release of IGF 1 could influence growth rate. CONCLUSIONS If three factors, namely rapid growth of Arctic deer in summer, photoperiodic timing of growth via IGF 1 and the rate of growth control via the amplitude of the increase in IGF 1 are taken together then there is a possible mechanism for the rapid summer growth which is observed in Arctic deer. It is proposed that high summer IGF 1, during ultra-long summer days might, in part, be responsible for rapid growth. Clearly Arctic deer have many constraints on growth, for example feed supply, insect harassment, disturbance (e.g., oil industry developments) and migration, but Klein (1968) proposed that deer body size in Arctic depends on summer range quality. It is proposed that we can now add the following, the endocrine system responds to daylength cues to maximise growth rate over the period of great food abundance. This concept, if correct, adds a new dimension to seasonal control mechanisms, that of rate, in addition to timing. In some taxa, this factor could perhaps explain Bergmann's Rule, although not in the genus Rangifer. It is recognised that conclusions and hypotheses in the present manuscript rely on data derived from "constant daylength" studies which, although straight forward to interpret in a cause-effect context, in no way represent the natural situation. This dilemma awaits further testing. Likewise, the endocrine mechanism to facilitate rapid growth during the brief summer period has been based on temperate deer studies, and should be tested in Arctic deer. In conclusion, with increasing latitude deer grow most during summer daylength which may influence both the timing of this growth and its rate via the amplitude of the summer elevation of IGF 1. REFERENCES Asher, G. W Growth and feeding management of farmed fallow deer in New Zealand. In G. W. Asher (ed.), Procs. First World Forum on Fallow Deer Farming, Mudgee, NSW, Australia

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