The male effect in indigenous Muzaffarnagari sheep. 1. Behavioural and ovarian responses of anoestrous ewes to male introduction

Abstract

In order to study the ‘male effect’ in postpartum anoestrous Muzaffarnagari ewes, 18 ewes were divided as per age, body weight, body condition score and body size into three equal groups, viz., teased with ram; buck and none (E; control). Teasing was done for 15 days at 122.3±50.1 days postpartum by intact, sexually experienced and aproned males. The ram was significantly (P<0.05) more effective in inducing oestrus than buck in respect of number of ewes in heat and increasing oestrus intensity score. The present study confirmed that the ‘male effect’ existed in Muzaffarnagari sheep.

Keywords:

• male effect
• Muzaffarnagari sheep
• ram effect
• buck effect
• oestrus intensity
• oestrus induction
• anoestrus

Introduction

The induction of cyclic reproductive activity in females well before the initiation of spontaneous cycling by introduction of males is characteristically known as ‘male effect’. This response is widely used to advance and synchronise breeding in sheep (Rosa and Bryant 2002). The ‘male effect’ is now one of the well established means of the small ruminant production without using much criticised hormonal therapy in today's health-conscious developed world.

The present study was conceptualised on the basis of the collected information that there exists an inter-specific pheromonal reaction in sheep and goats. Therefore, the present investigation was conducted to elucidate the ‘male effect’ in anoestrous indigenous ewes during post-partum by their ovarian and behavioural responses.

Materials and methods

The present study was conducted at Sheep and Goat Farm of Livestock Production Management Section, Indian Veterinary Research Institute, Izatnagar, India. A total of 18 Muzaffarnagari ewes (2.94±0.18 years, 33.8±1 kg, 3.12±0.17 BCS) of unusually long post-partum anoestrus and two entire sexually experienced males (one buck and one ram) were selected based on the age, body weight, body size, body condition score and sex steroid concentrations (testosterone in males and progesterone in females). The ewes were equally divided into three groups: Control (E): no male; Treatment 1 (ER): with ram; and Treatment 2 (EB): with buck. The males were associated with ewes for 15 days and the duration of observation on females in this experiment was 1 month after male introduction. The housing and feeding were kept identical in the given farm condition.

Before the experiment, the males were completely isolated (smell, sight and sound) from the females by providing 100 m away housing with specially curtained paddocks for 3 months. The various ovarian and behavioural parameters recorded were post-exposure interval to behavioural oestrus, proportion of females showing oestrus, proportion of females that ovulated, duration of oestrus, duration of standing oestrus and oestrus intensity score. The oestrus onset was confirmed from the interaction of oestrous female with aproned male that was specifically introduced with oestrous female for a brief period (15 min) at 4-h interval for the purpose. The animals were monitored continuously for 24 h for the precise behavioural recordings. The oestrus intensity score was assigned to the individual female according to a previously described method after suitable modification (Dhali et al. 2006). The criteria for assigning oestrus intensity score are described in Table 1. The ovulation in females was confirmed from serum progesterone level during the peri-oestrus period.

Table 1.  Scoring the oestrus intensity in indigenous ewes.

Female behavioural signs and activities	Male behaviour	OIS	Oestrus intensity
No overt oestrus signs, mild swelling in vulva may be seen occasionally	Sniffing, occasional flehmen (once in 15 min), orientation in female's proximity throughout but showing only occasional interest	1	Very weak
Occasional and low vocalisation or no vocalisation, mild restlessness, low intensity of male seeking, low to moderate tail fanning, swollen and pinkish vulva	Readily follows female, shows interest, sniffing and flehmen (twice in 15 min), remains within < 1 m of female	2	Weak
Rhythmic and loud vocalisation, restlessness, excitedness, tail fanning, moderately intense male seeking, ears erect, eyes fixed on male/doors, oedematous and red vulva, occasional secretion	No need for male use. If used, intense following, showing intense interest, sniffing, flehmen (>3 times), leg kicking, vocalisation, intense mounting intentions, and so on.	3	Moderate/normal
Intense vocalisation, rising early in the morning, very excited, intensely restless, tail fanning vigourously, trying to lick own genitalia, intense male seeking, oedematous, moist and red vulva, threadlike clear vaginal discharge	Do; mounting intensifies	4	Strong
Intense vocalisation, rising early in the morning, very very excited, intensely restless, vigorous tail fanning, trying to lick own genitalia, intense male seeking, mounting and mounted, turning head back, oedematous, moist and reddish vulva, vaginal discharge clear	Do; mounting intensifies further	5	Very strong
OIS: Oestrus Intensity Score.

The jugular vein blood samples (3 ml) were collected from the animals on day 10, 7 and 3 prior to male introduction and on day 0, 1, 2, 3, 4 and 5 following the male introduction. The serum samples were harvested and stored at −30°C until the estimations of testosterone and progesterone by radioimmunoassay (RIA). For ascertaining the date of ovulation, the progesterone concentration more than 0.5 ng/ml following the expression of behavioural oestrus and its continuous rise was pointed. The serum concentrations of progesterone and testosterone were estimated using the commercially available RIA kits (Immunotech®, Beckman Coulter Company, Marseille, France).

SPSS® 11.00 (2001) statistical package was used for the analysis. The chi-square was applied to test differences among the percentages and frequencies as per the standard procedure (Steel and Torrie 1981).

Results and discussion

The ewes were at 122.33±50.10 days post-partum and all of them were in anoestrous condition (serum P₄ level = 0.35±0.12 ng/ml). More ewes (P<0.05) teased with ram showed (Table 2) behavioural oestrus (100%) than those teased with buck (67%) or none (33%). The oestrus duration, standing heat length and oestrus intensity (Table 2) were improved (P<0.05) by introduction of male, ram did not differ (P>0.05) from buck for these parameters. Within 2 days, ram induced heat in more ewes (P<0.05) than buck (Table 2) indicating higher early synchronisation of oestrus incidence. A significant increase (P<0.05) in proportion of females ovulating and coming into heat, while joined with males indicated the existence of ‘male effect’ in indigenous breed of sheep. Aproned males used in the study were effective enough to induce and synchronise the oestrus in females to a considerable extent. Unlike other classical studies (Rosa and Bryant 2002), ewes were not showing any silent ovulation or anovulatory oestrus and this might be attributed to the environmental variation of the location of studies.

Table 2.  Effect of male introduction on oestrus and ovulatory responses of anoestrous ewes.

Attributes	Gr. I (E)	Gr. II (EB)	Gr. III (ER)
1. Ewes treated (n)	6	6	6
2. Ewes showing behavioural oestrus	2^A	4^B	6^C
3. Ewes ovulating	2^A	4^B	6^C
4. Post-exposure interval to oestrus (d)	25.00±1.00^a	4.50±1.19^b	2.67±.0.92^b
5. Post-exposure interval to ovulation (d)	26.87±0.87^a	5.85±1.14^b	3.58±0.90^b
6. Oestrus duration (h)	38.00±2.00^a	22.00±2.04^b	17.33±1.67^b
7. Oestrus intensity score (1–5 scale)	1.50±0.50^a	2.25±0.48^a	4.00±0.26^b
8. Duration of standing oestrus (h)	6.65±0.15^a	5.55±0.20^a	3.71±0.36^b
9. Degree of synchronisation
(1) Within 48 h	0^A	1^B	4^C
(2) Between 48 and 72 h	0	1	1
(3) After 72 h	2	2	1
Notes: E: ewes without male; ER: ewes teased with ram; EB: ewes teased with buck.
^A–CFigures with dissimilar superscripts in a row differed significantly (P<0.05).
^a,bMeans with dissimilar superscripts in a row differed significantly (P<0.05).

The postexposure interval to overt oestrus and that to ovulation were longer (P<0.05) in nonteased group (Table 2) than buck-teased and ram-teased groups. The significant effects of male introduction to the flock of anoestrous ewes on the heat length, duration of standing heat and the oestrus intensity score had been shown. The standing heat duration was affected (P<0.05) by presence of ram or buck. This variation might be attributed to the complex neural mechanisms that regulate the endocrine events involved in variation of the length of standing heat in ewes. However, paucity of similar kind of literature led to inability to compare the present findings. On the whole, the present findings corroborated with the earlier results (Rosa et al. 2000). The progesterone concentration (Figure 1) in ewes was in the similar trend as reported by Rosa et al. (2000) and Ungerfeld (2003).

Figure 1.  Serum progesterone concentration (ng/ml) in relation to ovine oestrus and ovulation induced by ‘male effect’.

However, in this experiment the novel use of aproned buck proved to be a little inferior to the aproned ram and that might be due to the fact that the social signals emitted by the buck could not have the ability to sensitise for incidence of overt oestrus in ewes (Mondal et al. 2006). Overall, the present findings indicated the effectiveness of buck and ram in inducing and synchronising the oestrus in postpartum anoestrous ewes.

Acknowledgements

The first author is highly grateful to the Director, National Research Centre on Mithun, Nagaland and the Director, Indian Veterinary Research Institute for extending co-operation and encouragements for taking up such studies. The financial help from Indian Council of Agricultural Research is duly acknowledged.

Additional information

Notes on contributors

S.K. Mondal

Part of Doctoral thesis submitted by S.K. Mondal