Studies of seasonality in red deer (Cervus elaphus) : with special emphasis on the reproductive physiology of red deer hinds

Abstract

Four trials were conducted to investigate factors controlling the seasonal onset of reproductive activity in red deer hinds.

Firstly (Chapter 4), the role of photorefractoriness to long daily photoperiods in the initiation of the seasonal reproductive activity in breeding red deer hinds was examined. Red deer hinds (n=10) were prematurely exposed to a long daily photoperiod of 15.3 h from 22 July to 8 November 1986 i.e. winter-spring (EPW), or maintained under natural photoperiods (NP). Six hinds experienced the natural changes in daily photoperiod until mid-summer but were exposed to a 15.5 h of light each day from 30 January to 30 April 1987, i.e. summer-autumn (EPS), whilst hinds in the other groups experienced naturally decreasing daily photoperiods. On 5 occasions (July 1986, January, February, March and April 1987), blood samples were collected from 4 NP and 4 EPW hinds every 20 minutes for 4 h to monitor secretion of luteinising hormone and half hourly for another 4 h following an i.v. injection of 2 µg GnRH to measure pituitary responsiveness. In January, March and April 1987 EPS hinds were also intensively sampled for 4 h. Plasma progesterone concentrations and mean date of calving indicated that the onset of breeding activity was not affected by light treatment in the EPW hinds but was delayed by 3 weeks in the EPS hinds. In contrast, supplementary lighting caused a premature elevation of plasma prolactin concentrations and advanced pelage moulting in EPW hinds only. Plasma LH secretion patterns indicated that LH pulse frequency and mean LH concentrations were greater during the breeding season than during pregnancy or, seasonal or postpartum, anoestrus. The reduction in LH secretion was partially explained by a diminished pituitary responsiveness to GnRH. Daily plasma melatonin secretion patterns indicated that the duration of the nocturnal increase in melatonin concentrations was responsive to changes in photoperiod and provided a suitable endocrine signal for measuring day length. The results suggest that, unlike the sheep and prepubertal red deer hind, the onset of seasonal breeding activity in breeding red deer hinds is not affected by long daily photoperiods in spring but is delayed if the autumnal decrease in daily photoperiod is delayed. Therefore neither the development of photorefractoriness nor the spring increase in daily photoperiods initiated the transition from seasonal anoestrus to reproductive activity in the breeding hind. However, long daily photoperiods may have entrained the annual cycle of pelage shedding and prolactin secretion. It is possible that the neuroendocrine pathway by which photoperiodic signals entrain the seasonal cycle of reproduction is separate from those which regulate other seasonal events in the breeding red deer hind.

Secondly (Chapter 5), in a study of seasonality of reproduction, 4 pubertal hinds were monitored for live weight and plasma LH and progesterone concentrations from December 1987 to October 1988 (i.e. 12-22 months of age). In addition the pattern of LH secretion was also studied in 4 ovariectomised pubertal hinds implanted s.c. with controlled release implants containing 12 mg oestradiol-17β between 4 March and 25 May and between 15 June and 19 September, 1988. On several occasions (15 December, 29 February, 15 March, 24 April, 14 June, 29 June, 18 September (all hinds) and 3 October (ovariectomised hinds only) blood samples were collected every 20 minutes for 4 h to monitor secretion of luteinising hormone and following an i.v. injection of 2 µg GnRH to measure pituitary responsiveness. Plasma progesterone profiles indicated that 4-6 ovarian cycles, lasting about 19 d each, occurred in each intact hind. Regular ovarian cycles commenced in late April (26 April ± 3.4 d, mean ± s.e.m.) and ceased 3 months later in July (21 July ± 7.2 d). The number of LH pulses in the intact hinds was higher in June (1-2 pulses/4 h) than in the non-breeding season (< 1 pulse/4 h) probably due to a seasonal increase in GnRH secretion. It appears that the seasonal increase in LH pulsatility and onset of reproductive activity in the entire hinds were temporally related to a reduction in the sensitivity of LH secretion to the negative feedback effects of oestradiol in ovariectomised pubertal hinds.

In the third trial (Chapter 6), 20 male and 20 female red deer calves were immunised at birth against a melatonin conjugate or injected with adjuvant only (controls). Booster injections were given on 5 occasions over the next 2 years. Stags which produced significant melatonin binding activity in response to immunisation, were heavier than the controls between 7 and 11 months of age and at 16, 20, 30 and 34 months of age. A similar but smaller effect on live weight was seen in the immunised hinds. Immunisation against melatonin did not affect the calving date of the hinds or antler development and time of casting of antlers in the stags. These results indicated that disruption of the photoperiodic signal by immunisation against melatonin may have prevented the entrainment of annual rhythms in feed intake and growth but without affecting the seasonal cycles in antler growth and ovarian activity.

Finally in a series of 3 trials (Chapter 7), anoestrous red deer hinds were induced to ovulate with the GnRH analogue, buserelin. Hinds were pre-treated with intravaginal devices containing 0.6 g progesterone (CIDR-Type S) for 14 days prior to CIDR withdrawal on 4 March. In Year 1, 15 hinds were treated with 1 CIDR each and 8 hinds were injected i.m. with 4 µg buserelin (a GnRH analogue) at CIDR removal followed by 2nd injection of 10 µg 48 h later. In Year 2, 16 hinds were treated with 2 CIDRs each and 8 hinds were injected Lm. with 4, 3, 2, 2 and 10 µg buserelin at -48, -24, 0, 24 and 48 h respectively from CIDR withdrawal. In Year 3, 15 hinds were treated with 2 CIDRs and 11 hinds (Groups Band BO) injected with buserelin identical to the protocol in Year 2. At CIDR withdrawal 6 of these buserelin treated hinds (Group BO) and 4 other progesterone-primed hinds (Group 0) were injected with 500 µg oestradiol benzoate. In addition, during the breeding season, 4 hinds (Group C) were treated with double CIDRs only for 14 d from 1 April. When oestrous behaviour and the pattern of plasma LH secretion were monitored in Year 3, oestrous behaviour was less noticeable and delayed in Group B hinds and peak LH levels were lower and increased later relative to Group 0, BO and C hinds. Two weeks after CIDR withdrawal, 6 buserelin-treated hinds in both Year 1 and Year 2, and 3/5 B, 2/4 0, 3/6 BO and 4/4 C group hinds in Year 3 had a single corpus luteum present. Plasma progesterone concentrations were elevated for about 12 d in most hinds with a corpus luteum in Year 2 and in most B, BO and C Group hinds in Year 3. However, progesterone secretion was low in several Year 1 and all Group 0 hinds in Year 3 indicating that the induced corpora lutea in these hinds were functionally subnormal. There was no evidence that any of the buserelin-induced ovulations resulted in pregnancy, probably because the induced ovulations were not accompanied by normal hormonal and behavioural patterns.

The experiments described in this thesis have contributed to our understanding of the regulation of seasonal breeding in red deer hinds. This knowledge may eventually enable reproductive activity to be effectively manipulated, thereby improving the efficiency of deer production systems.