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Relationship of age to seasonal levels of LH, FSH, prolactin and testosterone in male, white-tailed deer
Comp. Biochem. Physiol. Vol. 83A, No. 1, pp. 179-183, 1986 Printed in Great Britain
0300-9629/86 $3.00+0.00 ~ 1986 Pergamon Press Ltd
RELATIONSHIP OF AGE TO SEASONAL LEVELS OF LH, FSH, PROLACTIN AND TESTOSTERONE IN MALE, WHITE-TAILED DEER G. A. BUBENIK and D. SCHAMS Department of Zoology, University of Guelph, Guelph. Ontario, Canada, N1G 2W1; Telephone: (519)824-4120; and Department of Physiology, TU Munchen-Weihenstephan, D-805 Freising, F.R.G.
(Received 8 May 1985) Abstract--1. Seasonal levels of LH, FSH, Prolactin (PRL) and testosterone (T) were determined in blood plasma of penned male white-tailed deer, ranging in age from 2 to 10 yr. 2. Peak levels o f t (observed around the rutting season in November) gradually increased until the 7th yr and then they began to decline slowly; a sharp decrease was registered in the 10th yr. 3. Peak levels of PRL (measured in June) steadily increased until the 6th yr and then dropped rapidly in the 8-9-yr-old group. 4. Peak concentrations of FSH (observed during Septembe~October) rose gradually until the 6th yr, decreased in 8-yr-olds and then increased again in the 9th and 10th yr of life. 5. On the other hand LH maxima (occurring during July September) were rising until the 4th yr and then remained steady until the 6th yr. LH peaks in the 8th and 9th yr were more than 50% higher than that of the 4-6th yr. 6. These data indicate that increasing peak levels coincide with approaching "prime male age" around 5-7 yr. 7. In senior bucks (9 10 yr) decreasing gonadal function may be the sign of diminished responsiveness to pituitary hormones since gonadotrophins are elevated to the "castrate-type" levels.
INTRODUCTION White-tailed deer o f boreal regions are seasonal breeders a n d as such exhibit very distinct a n n u a l r h y t h m s o f g o n a d o t r o p i n s a n d sexual h o r m o n e s (McMillin et al., 1974; Bubenik et al., 1975; M i r a r c h i et a/., 1978; Bubenik et al., 1982). In virtually all male cervids investigated the peak seasonal levels o f sexual h o r m o n e s were f o u n d to vary considerably between individual animals of the same species (Barth et al., 1976; Bubenik et al., 1977; Lincoln a n d Kay, 1979; Schams a n d Barth, 1982; Haigh et al., 1984). It is assumed t h a t the highest levels are present in prime males o f the highest rank. However, this hypothesis was, to the best of o u r knowledge, never tested experimentally as ideally it does require a large n u m b e r o f animals o f k n o w n age a n d social rank to be investigated. Since the precise d e t e r m i n a t i o n of social r a n k is possible only by long-term observations (Bartos, 1981) and as the r a n k m i g h t change with such procedures as the removal o f antlers (Bubenik, 1968; Lincoln et al., 1970) (which is done in all our captive deer) we have decided to investigate only the effect of age on the levels of LH, FSH, Prolactin (PRL) a n d testosterone (T). MATERIALS AND METHODS
Twenty-one male white-tailed deer (Odocoileus virginianus) ranging in age from 2 to 10 yr kept first at the Ontario Please address all correspondence to: Dr. G. A. Bubenik, Ceasar Kleberg Wildl. Res. Inst., Dept. of Agriculture, Texas A and M University, Kingsville, TX 78363, U.S.A.
Ministry of Natural Resources Wildlife Compound in Midhurst (latitude 44.2 c') and later at the University of Guelph Deer Research Station in Cruikston Park, Cambridge, (latitude 43.4 °) were immobilized once a month using blowpipe and darts of our own design (Bubenik and Bubenik, 1978). The bucks were anaesthetized by 2-3 mg/kg of xylazine (Rompun) and then 50ml of blood were taken from the jugular vein. Some animals were sampled consecutively for up to 4 yr, others were sampled for 3-4 seasons, but with interruptions lasting one or more years. No blood samples were taken during the first year of life, as the reproductive cycles at that time differ from cycles in the following years (Suttie et al., 1984). A total of 53 cycles were investigated for seasonal levels of LH, FSH, PRL and T. Because of difficulties in deciding the ranks of our bucks, the hormonal values of deer of the same age were pooled in one group. The plasma levels of all hormones were determined by heterologous RIAs. LH was determined by a homologous bovine assay with no cross-reaction to other pituitary hormones. Sensitivity of the assay was 0.05 mg/tube, intra-assay coefficient of variation (CV) averaged 8.6~, and interassay variation was 11.5-19%. FSH was determined by a system where pure ovine FSH was used for labelling and antiserum against ovine FSH was raised in guinea pigs. The slight cross-reactivity with bovine LH and TSH was eliminated by adding a constant amount of LH to each tube. The sensitivity of the assay was 0.05 mg/tube. The intra-assay CV was 7.5~°~oand interassay variation was 12-18%. Prolactin was determined by homologous bovine assay. The antiserum raised in rabbits showed no cross-reactivity with other pituitary hormones. The sensitivity of the assay was 0.05 mg/tube. The intra-assay CV was 8.4% and the interassay CV was 14%. Testosterone was determined by a highly specific assay. The sensitivity of the assay was 50 pg/ml. The interassay CV was 7.5 12%. 179
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Fig. l. Seasonal levels of testosterone in 9 age groups of male white-tailed deer. Vertical bars indicate standard errors, n = number of animals in each group.
Details of radioimmunoassays are described in our previous papers (Bubenik et al., 1982; Bubenik et aL, 1983). The significance of seasonal peaks was determined by a Student's t-test.
peak T levels was registered in 10-yr-old bucks. Except for old bucks in their 10th yr of life, all other peak levels were significantly higher (P < 0.05) than basal values during spring. Prolactin (Fig. 2)
RESULTS
Peak PRL levels were reached in all age groups in June. There was a gradual increase in maximal levels from 2nd to 6th yr. Unfortunately there were not enough data available for the 7th yr and the age groups of 8th and 9th yr had to be evaluated together. A sharp drop in peak PRL levels was registered in the "senior" group (Sth-9th yr of life) (Bubenik, 1982). All peak levels of PRL were significantly higher (P < 0.05) than basal values in autumn and winter.
Testosterone (Fig. 1)
Testosterone results were the most complete of all hormones investigated, as there was enough data available to calculate average seasonal fluctuations for each of the 9 age groups. Peak levels were reached in November in all groups except the oldest one; however, the magnitude of the increase differs considerably. There was only a moderate increment in maximal T levels in the "teenage" group (2nd~,th yr) (Bubenik, 1982). A distinct category characterized by a high T level around the rutting season followed the group of younger bucks. In this group of"primes" (Bubenik, 1982) the highest levels of T were reached during the 7th yr of life, however relatively high T levels were maintained until the age of 9 yr. Then a dramatic decrease in
F S H (Fig. 3)
Peak levels of FSH were found in the September-October period. A slow increment of peak levels was observed between 2nd and 6th yr with a rapid decline in bucks in their 8th yr of life. However, very high levels of FSH (in the range found in castrates) were detected in the 9th yr of life.
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Fig. 3. Seasonal levels of FSH in six age groups of male white-tailed deer.
L H (Fig. 4)
Seasonal levels of LH exhibited the most variable pattern of all four hormones investigated. Maximal levels of LH were registered mostly in August; however, several peaks were also observed in June, July and September. The seasonal pattern of bucks in their 2nd and 3rd yr of life was the most irregular with peaks in August and July, respectively. In 4th-6th yr of life the seasonal increase was rather smooth with distinct peaks found earlier with advancing age. Again, the group of deer in their 7th yr of life was not available for calculation. However, sufficient data enabled us to calculate bucks in their 8th and 9th yr of life as separate groups. Surprisingly, peak LH levels (found in September and August, respectively) in this category of "seniors" were almost 50~o higher than in the "prime" group. It appears that with increasing age the seasonal pattern of LH becomes irregular once again.
Peak levels during the summer were significantly higher than winter and spring values only in bucks older than 3 yr. In the group of bucks between the 4th and 6th yr of life the level of significance was 0.02, in deer in their 8th and 9th yr the level was 0.05. DISCUSSION Based on the presumption that the peak levels of T found in plasma during the sensitive period around the rut are related to reproductive capacity of the male deer (Lincoln et al., 1972) several deductions can be made. First, white-tailed bucks do not reach the "prime" category before they are at least 5 yr old. Secondly, prime age culminates in the 7th and 8th yr, however, strong reproductive potential can be maintained until the bucks are about 9 yr old. Finally a rapid decline is expected around the 10th yr of life.
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9
182
G . A . BUBENIKand D. SCHAMS
These conclusions are supported by extensive behavioural observations of our experimental animals. A high level of excitability (so typical for juvenile white-tailed deer) is later replaced with a cautious attitude towards humans. The most distinct transition in the level of self confidence was observed in our animals between the 4th and 5th yr of life. On the other hand, aggressivity of tamed bucks towards humans (persisting between October and January) is most pronounced in 6-7-yr-olds. A remarkable decrease in aggressivity (we could enter the pen without the risk of being attacked) was observed in bucks after they reached their 10th yr of life. Two other signs of aging (known to be related to hypogonadism in white-tailed deer) such as superficial hyperostosis of main beams (known as "pearls") (Bubenik, 1966) and the lack of polishing drive (leading to persistence of dry velvet throughout the winter) (Thomas et al., 1965) were most obviously manifested after bucks reached their 9th yr of life. Seasonal changes of volume of red deer (C. elap h u s ) testes were found to be very similar to our findings of seasonal T levels in white-tailed deer. The highest seasonal volume was found in " p r i m e " stags, [e.g. 8 10-yr-olds (Lincoln, 1981)]. In our experimental white-tailed deer the corresponding age was 7 8 yr according to T data. It is evident that our data might be most relevant for the semi-tamed captive deer. Absolute levels as well as time course of T in wild bucks were found to be different from T in captive animals (Mirarchi et al., 1977). In addition these parameters might change with latitude, as the peak of the rut is different at various parts o f the North American continent (McMillin et al., 1974; Mirarchi et al., 1977; Brown et al., 1983). Lungmayr and Spona (1975) concluded that Leydig cells of old men exhibit primary hypergonadotrophic dysfunction. Basal T levels were found not to be different in aging men, however, the stimulation capacity of the testes decreased in men older than 60 yr. In humans, plasma levels of both FSH and LH were found to be higher in elderly men (Lungmayr and Spona, 1975; Touitou et al., 1983). The delayed increase of T in our "senior" bucks might be an indication of a diminished responsiveness of the gonads to the seasonal changes of pituitary hormones. In the red deer study (Lincoln, 198l) a sudden decrease in testes volume was registered in the last year of life. The high levels of LH and FSH might be the result of such an effect. The gonadotropin levels were in the same range as the ones observed in castrates in our previous study (Bubenik et al., 1982). The differences in timing of peak levels of FSH and LH indicates that both gonadotropins are regulated by separate feedback mechanisms as also shown for the roe deer buck (Schams and Barth, 1982). The marked increase of LH peak values in the 8th and 9th yr of life coincides with the onset of delay in rise of T in August. For the FSH in the 9- and 10-year-old animals other factors should be considered, perhaps related to diminished tubular function (changes in production of inhibin by Sertoli cells may be assumed). The sluggish rise o f T levels during summer in older bucks might be related to low peak levels of PRL in
that group. Strong relationships between PRL levels and timing of LH and T secretion in white-tailed deer were found in our previous study (Bubenik et al., 1986). Some evidence indicates that a withdrawal of P R L may modulate the occurrence of reproductive arrest in ruminants (Bittman, 1984). Prolactin is a hormone most sensitive to photoperiodic stimulation (Lincoln et al., 1978). This stimulation is mediated by the pineal gland and its hormone melatonin (Smith et al., 1984). As a rapid decrease of peak diurnal levels of pineal and plasma melatonin was established in old male and female syrian hamsters (Reiter, 1975; Reiter et al., 1982), it can be speculated that such a decrease in sensitivity of the pineal to photoperiodic stimulation in our over aged bucks might have caused their low secretion or P R L in the spring.
REFERENCES
Barth V. D., Gimenez T., Hoffman B. and Karg H. (1976) Testosteronekonzentration im peripheren Nut beim rehbock (Capreolus capreolus). Z. Jagdwiss. 22, 134 148. Bartos L. (1981) Reproductive and social aspects of the behaviour of "white" red deer. Saugetierkundl. Mitt. 30, 89-117. Bittman E. L. (1984) Melatonin and photoperiodic time measurement: evidence from rodents and ruminants. In The Pineal Gland (Edited by Reiter R. J.), pp. 155 192. Raven Press, New York. Brown R. D., Chao C. C. and Faulkner L. W. (1983) The endocrine control of the initiation and growth of antlers in white-tailed deer. Acta endocr., Copnh. 103, 138 144. Bubenik A. B. (1966) Das Geweih, pp. 1-214. Paul Parey, Hamburg. Bubenik A. B. (1968) The significance of antlers in the social life of the Cervidae. Deer 1, 208 214. Bubenik A. B. (1982) Physiology of wapiti. In Elk of North America (Edited by Thomas J. W. and Toweill D. E.), pp. 125-179. Wildl. Manage. Inst., Washington, D.C. Bubenik A. B. and Bubenik G. A. (1978) New, nontraumatic, disposable, automatic injection dart. C.A.L.A.S. Proc., pp. 48-53. Bubenik G. A., Bubenik A. B., Brown G. M. and Wilson D. A. (1975) The role of sex hormones in the growth of antler bone tissue. 1. Endocrine and metabolic effects of antiandrogen therapy. J. exp. Zool. 194, 349-358. Bubenik B. A., Bubenik A. B., Brown G. M. and Wilson D. A. (1977) Sexual stimulation and variations of plasma testosterone in normal, antiandrogen and antiestrogen treated white-tailed deer (Odocoilues virginianus) during the annual cycle. Proc. 13th Inl. Congress of Game Biol.. Atlanta, GA, pp. 377-386. Bubenik G. A., Morris J. M., Schams D. and Claus A. (1982) Photoperiodicity and circannual levels of LH, FSH, and testosterone in normal and castrated male, white-tailed deer. Can. J. Physiol. Pharmac. 60, 788-793. Bubenik G. A., Bubenik A. B., Schams D. and Leatherland J. F. (1983) Circadian and circannual rhythms of LH, FSH, testosterone, prolactin, cortisol, T 3 and T 4 in plasma of mature, male white-tailed deer. Comp. Biochem. Physiol. 76A, 37-45. Bubenik G. A., Schams D. and Leatherland J. F. (1986) Prolactin studies in male white-tailed deer. In Biol. Deer Production (Edited by Drew K. and Fennessey P.). Royal Soc. of New Zealand and Invermay Agric. Res. Inst., Dunedin. (In press.) Haigh J. C., Cates W. F., Glover G. J., Rawlings N. C. (1984) Relationships between seasonal changes in serum testosterone concentrations, scrotal circumference and
Age and hormones in male deer sperm morphology of male wapiti (Cervus elaphus). J. Reprod. Fert. 70, 413-418. Lincoln G. A. (1981) Seasonal aspects of testicular function. In The Testis (Edited by Burger H. and de Kretser D.), pp. 255-302. Raven Press, New York. Lincoln G. A., Youngson R. W. and Short R. V. (1970) The social and sexual behaviour of the red deer stag. J. Reprod. Fert. Suppl. 11, 71-103. Lincoln G. A,, Guiness F. and Short R. V. (1972) The way which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Hormone Behav, 3, 375-396. Lincoln G. A., McNeilly A. S. and Cameron C. L. (1978) The effects of a sudden decrease in day-length on prolaetin secretion in the ram. J. Reprod. Fert. 52, 305-311. Lincoln G. A. and Kay R. N. B. (1979) Effects of season on the secretion of LH and testosterone in intact and castrated red deer stags ( Cervus elaphus ). J. Reprod. Fert. 55, 75-80. Lungmayr G. and Spona J. (1975) Pituitary and gonadal functional reserve of men as a function of age. Wien klin. Wschr. 87, 200-204. McMillin J. M., Seal U. S., Keenlyne K. D., Erickson A. W. and Jones J. E. (1974) Annual testosterone rhythm in the adult white-tailed deer (Odocoileus virginianus borealis). Endocrinology 94, 1034-1040. Mirarchi R. E., Scanlon P. F., Kirkpatrick R. L. and Schreck C. B. (1977) Androgen levels and antler development in captive and wild white-tailed deer. J. Wildl. Mgmt 41, 178-183.
183
Mirarchi R. E., Howland B. E., Scanlon P. F., Kirkpatrick R. L. and Sanford L. M. (1978) Seasonal variation in plasma LH, FSH, prolactin, and testosterone concentrations in adult male white-tailed deer. Can. J. Zool. 56, 121-127. Reiter R. J. (1975) Changes in pituitary prolactin levels of female hamsters as a function of age, photoperiods and pinealectomy. Acta Endocrinol. 79, 43-50. Reiter R. J., Vriend J., Brainard G. C., Matthews S. A. and Craft C. M. (1982) Reduced pineal and plasma melatonin levels and gonadal atrophy in old hamsters kept under winter photoperiods. Expl Ag. Res. 8, 27-30. Schams D. and Barth D. (1982) Annual profiles of reproductive hormones in peripheral plasma of the male roe deer (Capreolus capreolus). J. Reprod. Fert. 66, 463-468. Smith P. S., Bubenik G. A. and Schams D. (1984) The effects of orally administered melatonin (M) on the seasonal levels of deer LH, FSH, testosterone (T), prolactin (Prl), T3, T4, cortisol and M. J. Steroid Biochem. 20, 1464. Suttie J. M., Lincoln G. A. and Kay R. N. B. (1984) Endocrine control of antler growth in red deer stags. J. Reprod. Fert. 71, 7-15. Thomas J. W., Robinson R. M. and Marburger R. G. (1965) Social behavior in a white-tailed deer herd containing hypogonadal males. J. Mammal. 46, 314-327. Touitou Y., Lagoguey M., Bogdan A., Reinberg A. and Beck H. (1983) Seasonal rhythms of plasma gonadotrophins: their presence in the elderly men and women. J. Endocr. 96, 15-21.
0300-9629/86 $3.00+0.00 ~ 1986 Pergamon Press Ltd
RELATIONSHIP OF AGE TO SEASONAL LEVELS OF LH, FSH, PROLACTIN AND TESTOSTERONE IN MALE, WHITE-TAILED DEER G. A. BUBENIK and D. SCHAMS Department of Zoology, University of Guelph, Guelph. Ontario, Canada, N1G 2W1; Telephone: (519)824-4120; and Department of Physiology, TU Munchen-Weihenstephan, D-805 Freising, F.R.G.
(Received 8 May 1985) Abstract--1. Seasonal levels of LH, FSH, Prolactin (PRL) and testosterone (T) were determined in blood plasma of penned male white-tailed deer, ranging in age from 2 to 10 yr. 2. Peak levels o f t (observed around the rutting season in November) gradually increased until the 7th yr and then they began to decline slowly; a sharp decrease was registered in the 10th yr. 3. Peak levels of PRL (measured in June) steadily increased until the 6th yr and then dropped rapidly in the 8-9-yr-old group. 4. Peak concentrations of FSH (observed during Septembe~October) rose gradually until the 6th yr, decreased in 8-yr-olds and then increased again in the 9th and 10th yr of life. 5. On the other hand LH maxima (occurring during July September) were rising until the 4th yr and then remained steady until the 6th yr. LH peaks in the 8th and 9th yr were more than 50% higher than that of the 4-6th yr. 6. These data indicate that increasing peak levels coincide with approaching "prime male age" around 5-7 yr. 7. In senior bucks (9 10 yr) decreasing gonadal function may be the sign of diminished responsiveness to pituitary hormones since gonadotrophins are elevated to the "castrate-type" levels.
INTRODUCTION White-tailed deer o f boreal regions are seasonal breeders a n d as such exhibit very distinct a n n u a l r h y t h m s o f g o n a d o t r o p i n s a n d sexual h o r m o n e s (McMillin et al., 1974; Bubenik et al., 1975; M i r a r c h i et a/., 1978; Bubenik et al., 1982). In virtually all male cervids investigated the peak seasonal levels o f sexual h o r m o n e s were f o u n d to vary considerably between individual animals of the same species (Barth et al., 1976; Bubenik et al., 1977; Lincoln a n d Kay, 1979; Schams a n d Barth, 1982; Haigh et al., 1984). It is assumed t h a t the highest levels are present in prime males o f the highest rank. However, this hypothesis was, to the best of o u r knowledge, never tested experimentally as ideally it does require a large n u m b e r o f animals o f k n o w n age a n d social rank to be investigated. Since the precise d e t e r m i n a t i o n of social r a n k is possible only by long-term observations (Bartos, 1981) and as the r a n k m i g h t change with such procedures as the removal o f antlers (Bubenik, 1968; Lincoln et al., 1970) (which is done in all our captive deer) we have decided to investigate only the effect of age on the levels of LH, FSH, Prolactin (PRL) a n d testosterone (T). MATERIALS AND METHODS
Twenty-one male white-tailed deer (Odocoileus virginianus) ranging in age from 2 to 10 yr kept first at the Ontario Please address all correspondence to: Dr. G. A. Bubenik, Ceasar Kleberg Wildl. Res. Inst., Dept. of Agriculture, Texas A and M University, Kingsville, TX 78363, U.S.A.
Ministry of Natural Resources Wildlife Compound in Midhurst (latitude 44.2 c') and later at the University of Guelph Deer Research Station in Cruikston Park, Cambridge, (latitude 43.4 °) were immobilized once a month using blowpipe and darts of our own design (Bubenik and Bubenik, 1978). The bucks were anaesthetized by 2-3 mg/kg of xylazine (Rompun) and then 50ml of blood were taken from the jugular vein. Some animals were sampled consecutively for up to 4 yr, others were sampled for 3-4 seasons, but with interruptions lasting one or more years. No blood samples were taken during the first year of life, as the reproductive cycles at that time differ from cycles in the following years (Suttie et al., 1984). A total of 53 cycles were investigated for seasonal levels of LH, FSH, PRL and T. Because of difficulties in deciding the ranks of our bucks, the hormonal values of deer of the same age were pooled in one group. The plasma levels of all hormones were determined by heterologous RIAs. LH was determined by a homologous bovine assay with no cross-reaction to other pituitary hormones. Sensitivity of the assay was 0.05 mg/tube, intra-assay coefficient of variation (CV) averaged 8.6~, and interassay variation was 11.5-19%. FSH was determined by a system where pure ovine FSH was used for labelling and antiserum against ovine FSH was raised in guinea pigs. The slight cross-reactivity with bovine LH and TSH was eliminated by adding a constant amount of LH to each tube. The sensitivity of the assay was 0.05 mg/tube. The intra-assay CV was 7.5~°~oand interassay variation was 12-18%. Prolactin was determined by homologous bovine assay. The antiserum raised in rabbits showed no cross-reactivity with other pituitary hormones. The sensitivity of the assay was 0.05 mg/tube. The intra-assay CV was 8.4% and the interassay CV was 14%. Testosterone was determined by a highly specific assay. The sensitivity of the assay was 50 pg/ml. The interassay CV was 7.5 12%. 179
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Fig. l. Seasonal levels of testosterone in 9 age groups of male white-tailed deer. Vertical bars indicate standard errors, n = number of animals in each group.
Details of radioimmunoassays are described in our previous papers (Bubenik et al., 1982; Bubenik et aL, 1983). The significance of seasonal peaks was determined by a Student's t-test.
peak T levels was registered in 10-yr-old bucks. Except for old bucks in their 10th yr of life, all other peak levels were significantly higher (P < 0.05) than basal values during spring. Prolactin (Fig. 2)
RESULTS
Peak PRL levels were reached in all age groups in June. There was a gradual increase in maximal levels from 2nd to 6th yr. Unfortunately there were not enough data available for the 7th yr and the age groups of 8th and 9th yr had to be evaluated together. A sharp drop in peak PRL levels was registered in the "senior" group (Sth-9th yr of life) (Bubenik, 1982). All peak levels of PRL were significantly higher (P < 0.05) than basal values in autumn and winter.
Testosterone (Fig. 1)
Testosterone results were the most complete of all hormones investigated, as there was enough data available to calculate average seasonal fluctuations for each of the 9 age groups. Peak levels were reached in November in all groups except the oldest one; however, the magnitude of the increase differs considerably. There was only a moderate increment in maximal T levels in the "teenage" group (2nd~,th yr) (Bubenik, 1982). A distinct category characterized by a high T level around the rutting season followed the group of younger bucks. In this group of"primes" (Bubenik, 1982) the highest levels of T were reached during the 7th yr of life, however relatively high T levels were maintained until the age of 9 yr. Then a dramatic decrease in
F S H (Fig. 3)
Peak levels of FSH were found in the September-October period. A slow increment of peak levels was observed between 2nd and 6th yr with a rapid decline in bucks in their 8th yr of life. However, very high levels of FSH (in the range found in castrates) were detected in the 9th yr of life.
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Fig. 2. Seasonal levels of prolactin in six age groups of male white-tailed deer.
Age and hormones in male deer
181
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Fig. 3. Seasonal levels of FSH in six age groups of male white-tailed deer.
L H (Fig. 4)
Seasonal levels of LH exhibited the most variable pattern of all four hormones investigated. Maximal levels of LH were registered mostly in August; however, several peaks were also observed in June, July and September. The seasonal pattern of bucks in their 2nd and 3rd yr of life was the most irregular with peaks in August and July, respectively. In 4th-6th yr of life the seasonal increase was rather smooth with distinct peaks found earlier with advancing age. Again, the group of deer in their 7th yr of life was not available for calculation. However, sufficient data enabled us to calculate bucks in their 8th and 9th yr of life as separate groups. Surprisingly, peak LH levels (found in September and August, respectively) in this category of "seniors" were almost 50~o higher than in the "prime" group. It appears that with increasing age the seasonal pattern of LH becomes irregular once again.
Peak levels during the summer were significantly higher than winter and spring values only in bucks older than 3 yr. In the group of bucks between the 4th and 6th yr of life the level of significance was 0.02, in deer in their 8th and 9th yr the level was 0.05. DISCUSSION Based on the presumption that the peak levels of T found in plasma during the sensitive period around the rut are related to reproductive capacity of the male deer (Lincoln et al., 1972) several deductions can be made. First, white-tailed bucks do not reach the "prime" category before they are at least 5 yr old. Secondly, prime age culminates in the 7th and 8th yr, however, strong reproductive potential can be maintained until the bucks are about 9 yr old. Finally a rapid decline is expected around the 10th yr of life.
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Year o f Life Fig. 4. Seasonal levels o f L H in seven age groups o f ma|e white-tailed deer.
9
182
G . A . BUBENIKand D. SCHAMS
These conclusions are supported by extensive behavioural observations of our experimental animals. A high level of excitability (so typical for juvenile white-tailed deer) is later replaced with a cautious attitude towards humans. The most distinct transition in the level of self confidence was observed in our animals between the 4th and 5th yr of life. On the other hand, aggressivity of tamed bucks towards humans (persisting between October and January) is most pronounced in 6-7-yr-olds. A remarkable decrease in aggressivity (we could enter the pen without the risk of being attacked) was observed in bucks after they reached their 10th yr of life. Two other signs of aging (known to be related to hypogonadism in white-tailed deer) such as superficial hyperostosis of main beams (known as "pearls") (Bubenik, 1966) and the lack of polishing drive (leading to persistence of dry velvet throughout the winter) (Thomas et al., 1965) were most obviously manifested after bucks reached their 9th yr of life. Seasonal changes of volume of red deer (C. elap h u s ) testes were found to be very similar to our findings of seasonal T levels in white-tailed deer. The highest seasonal volume was found in " p r i m e " stags, [e.g. 8 10-yr-olds (Lincoln, 1981)]. In our experimental white-tailed deer the corresponding age was 7 8 yr according to T data. It is evident that our data might be most relevant for the semi-tamed captive deer. Absolute levels as well as time course of T in wild bucks were found to be different from T in captive animals (Mirarchi et al., 1977). In addition these parameters might change with latitude, as the peak of the rut is different at various parts o f the North American continent (McMillin et al., 1974; Mirarchi et al., 1977; Brown et al., 1983). Lungmayr and Spona (1975) concluded that Leydig cells of old men exhibit primary hypergonadotrophic dysfunction. Basal T levels were found not to be different in aging men, however, the stimulation capacity of the testes decreased in men older than 60 yr. In humans, plasma levels of both FSH and LH were found to be higher in elderly men (Lungmayr and Spona, 1975; Touitou et al., 1983). The delayed increase of T in our "senior" bucks might be an indication of a diminished responsiveness of the gonads to the seasonal changes of pituitary hormones. In the red deer study (Lincoln, 198l) a sudden decrease in testes volume was registered in the last year of life. The high levels of LH and FSH might be the result of such an effect. The gonadotropin levels were in the same range as the ones observed in castrates in our previous study (Bubenik et al., 1982). The differences in timing of peak levels of FSH and LH indicates that both gonadotropins are regulated by separate feedback mechanisms as also shown for the roe deer buck (Schams and Barth, 1982). The marked increase of LH peak values in the 8th and 9th yr of life coincides with the onset of delay in rise of T in August. For the FSH in the 9- and 10-year-old animals other factors should be considered, perhaps related to diminished tubular function (changes in production of inhibin by Sertoli cells may be assumed). The sluggish rise o f T levels during summer in older bucks might be related to low peak levels of PRL in
that group. Strong relationships between PRL levels and timing of LH and T secretion in white-tailed deer were found in our previous study (Bubenik et al., 1986). Some evidence indicates that a withdrawal of P R L may modulate the occurrence of reproductive arrest in ruminants (Bittman, 1984). Prolactin is a hormone most sensitive to photoperiodic stimulation (Lincoln et al., 1978). This stimulation is mediated by the pineal gland and its hormone melatonin (Smith et al., 1984). As a rapid decrease of peak diurnal levels of pineal and plasma melatonin was established in old male and female syrian hamsters (Reiter, 1975; Reiter et al., 1982), it can be speculated that such a decrease in sensitivity of the pineal to photoperiodic stimulation in our over aged bucks might have caused their low secretion or P R L in the spring.
REFERENCES
Barth V. D., Gimenez T., Hoffman B. and Karg H. (1976) Testosteronekonzentration im peripheren Nut beim rehbock (Capreolus capreolus). Z. Jagdwiss. 22, 134 148. Bartos L. (1981) Reproductive and social aspects of the behaviour of "white" red deer. Saugetierkundl. Mitt. 30, 89-117. Bittman E. L. (1984) Melatonin and photoperiodic time measurement: evidence from rodents and ruminants. In The Pineal Gland (Edited by Reiter R. J.), pp. 155 192. Raven Press, New York. Brown R. D., Chao C. C. and Faulkner L. W. (1983) The endocrine control of the initiation and growth of antlers in white-tailed deer. Acta endocr., Copnh. 103, 138 144. Bubenik A. B. (1966) Das Geweih, pp. 1-214. Paul Parey, Hamburg. Bubenik A. B. (1968) The significance of antlers in the social life of the Cervidae. Deer 1, 208 214. Bubenik A. B. (1982) Physiology of wapiti. In Elk of North America (Edited by Thomas J. W. and Toweill D. E.), pp. 125-179. Wildl. Manage. Inst., Washington, D.C. Bubenik A. B. and Bubenik G. A. (1978) New, nontraumatic, disposable, automatic injection dart. C.A.L.A.S. Proc., pp. 48-53. Bubenik G. A., Bubenik A. B., Brown G. M. and Wilson D. A. (1975) The role of sex hormones in the growth of antler bone tissue. 1. Endocrine and metabolic effects of antiandrogen therapy. J. exp. Zool. 194, 349-358. Bubenik B. A., Bubenik A. B., Brown G. M. and Wilson D. A. (1977) Sexual stimulation and variations of plasma testosterone in normal, antiandrogen and antiestrogen treated white-tailed deer (Odocoilues virginianus) during the annual cycle. Proc. 13th Inl. Congress of Game Biol.. Atlanta, GA, pp. 377-386. Bubenik G. A., Morris J. M., Schams D. and Claus A. (1982) Photoperiodicity and circannual levels of LH, FSH, and testosterone in normal and castrated male, white-tailed deer. Can. J. Physiol. Pharmac. 60, 788-793. Bubenik G. A., Bubenik A. B., Schams D. and Leatherland J. F. (1983) Circadian and circannual rhythms of LH, FSH, testosterone, prolactin, cortisol, T 3 and T 4 in plasma of mature, male white-tailed deer. Comp. Biochem. Physiol. 76A, 37-45. Bubenik G. A., Schams D. and Leatherland J. F. (1986) Prolactin studies in male white-tailed deer. In Biol. Deer Production (Edited by Drew K. and Fennessey P.). Royal Soc. of New Zealand and Invermay Agric. Res. Inst., Dunedin. (In press.) Haigh J. C., Cates W. F., Glover G. J., Rawlings N. C. (1984) Relationships between seasonal changes in serum testosterone concentrations, scrotal circumference and
Age and hormones in male deer sperm morphology of male wapiti (Cervus elaphus). J. Reprod. Fert. 70, 413-418. Lincoln G. A. (1981) Seasonal aspects of testicular function. In The Testis (Edited by Burger H. and de Kretser D.), pp. 255-302. Raven Press, New York. Lincoln G. A., Youngson R. W. and Short R. V. (1970) The social and sexual behaviour of the red deer stag. J. Reprod. Fert. Suppl. 11, 71-103. Lincoln G. A,, Guiness F. and Short R. V. (1972) The way which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Hormone Behav, 3, 375-396. Lincoln G. A., McNeilly A. S. and Cameron C. L. (1978) The effects of a sudden decrease in day-length on prolaetin secretion in the ram. J. Reprod. Fert. 52, 305-311. Lincoln G. A. and Kay R. N. B. (1979) Effects of season on the secretion of LH and testosterone in intact and castrated red deer stags ( Cervus elaphus ). J. Reprod. Fert. 55, 75-80. Lungmayr G. and Spona J. (1975) Pituitary and gonadal functional reserve of men as a function of age. Wien klin. Wschr. 87, 200-204. McMillin J. M., Seal U. S., Keenlyne K. D., Erickson A. W. and Jones J. E. (1974) Annual testosterone rhythm in the adult white-tailed deer (Odocoileus virginianus borealis). Endocrinology 94, 1034-1040. Mirarchi R. E., Scanlon P. F., Kirkpatrick R. L. and Schreck C. B. (1977) Androgen levels and antler development in captive and wild white-tailed deer. J. Wildl. Mgmt 41, 178-183.
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Mirarchi R. E., Howland B. E., Scanlon P. F., Kirkpatrick R. L. and Sanford L. M. (1978) Seasonal variation in plasma LH, FSH, prolactin, and testosterone concentrations in adult male white-tailed deer. Can. J. Zool. 56, 121-127. Reiter R. J. (1975) Changes in pituitary prolactin levels of female hamsters as a function of age, photoperiods and pinealectomy. Acta Endocrinol. 79, 43-50. Reiter R. J., Vriend J., Brainard G. C., Matthews S. A. and Craft C. M. (1982) Reduced pineal and plasma melatonin levels and gonadal atrophy in old hamsters kept under winter photoperiods. Expl Ag. Res. 8, 27-30. Schams D. and Barth D. (1982) Annual profiles of reproductive hormones in peripheral plasma of the male roe deer (Capreolus capreolus). J. Reprod. Fert. 66, 463-468. Smith P. S., Bubenik G. A. and Schams D. (1984) The effects of orally administered melatonin (M) on the seasonal levels of deer LH, FSH, testosterone (T), prolactin (Prl), T3, T4, cortisol and M. J. Steroid Biochem. 20, 1464. Suttie J. M., Lincoln G. A. and Kay R. N. B. (1984) Endocrine control of antler growth in red deer stags. J. Reprod. Fert. 71, 7-15. Thomas J. W., Robinson R. M. and Marburger R. G. (1965) Social behavior in a white-tailed deer herd containing hypogonadal males. J. Mammal. 46, 314-327. Touitou Y., Lagoguey M., Bogdan A., Reinberg A. and Beck H. (1983) Seasonal rhythms of plasma gonadotrophins: their presence in the elderly men and women. J. Endocr. 96, 15-21.