Two or 24 h of daily contact with sexually active males results in different profiles of LH secretion that both lead to ovulation in anestrous goats
Introduction
In breeds of ewes and goats showing reproductive seasonality, there is an alternation between breeding and anestrous seasons under the main control of photoperiod. During the season of sexual rest, the introduction of a male into a group of females in seasonal anestrus can rapidly induce an increase in levels of plasma luteinizing hormone (LH) leading to ovulation within 72 h [1], [2], [3], [4], [5]. This sexual stimulation, known as the “male effect,” has been extensively studied in ewes [1], [6], [7], [8] and goats [9], [10], [11].
The secretion of LH and ovulation in females exposed to the male can be influenced by factors such as duration of male contact and intensity of the males' sexual behavior. Since the earliest studies, it has been thought that continuous presence of the male is required to maximize the endocrine and ovulatory responses of females exposed to the male stimulus [12], [13]. In both goats and ewes, exposure to males induces secretion of LH within 15 min, but the stimulation of ovulation requires a greater duration of contact between sexes [14], [15], [16], [17]. Indeed, it has been shown that as soon as the male is withdrawn, secretion of LH decreases [13]. These results suggest that the presence of the male must be continuous (ie, 24 h/d) to maintain secretion of LH sufficient for ovulation [13], [18]. In fact, only 18% of ewes ovulated when exposed to males for 24 h, whereas 53% and 61% ovulated when males were maintained for 4 and 15 d, respectively [15].
Recently, we showed that it is possible to decrease the duration of daily contact between sexes without reducing the ovulatory response in goats. In fact, most females ovulated (>85%) when exposed to males 4 h/d during 15 consecutive days and this percentage was similar to that of females in permanent contact (24 h/d) with males [19], [20], [21]. Moreover, those recent studies also showed that ovulation rates were not reduced when the duration of daily contact is decreased [20], [21].
A likely explanation is that bucks rendered sexually active by photoperiodic treatment of long days were used in these studies. Indeed, it was found in both goats and ewes, that an intense sexual behavior of males is a key component to induce most females to ovulate by means of the male effect [19], [22], [23]. In female goats, pulsatility of LH remained elevated at least 24 h when in contact with a photoperiodic-treated buck displaying an intense sexual behavior [17]. In contrast, females in contact with a sedated similarly treated buck (sexually inactive) had decreased pulsatility of LH after the first 4 h of buck exposure [17]. Finally, the proportion of females that ovulated when exposed to photoperiodic-treated bucks was greater than that of females exposed to the sedated photoperiodic-treated bucks (95% vs 0%, respectively) [24].
On the basis of our previous results with sexually active bucks, we performed two experiments to determine (1) whether sexually active males are able to stimulate the sexual activity of anestrous female goats when duration of contact is further reduced from 4 to 2 or 1 daily hour during 15 d and (2) the pattern of secretion of LH when anestrous goats are exposed continuously (24 h/d) or intermittently (2 h/d) to males for 5 d.
Section snippets
Conditions of the studies
Two experiments were carried out during the nonbreeding season using local goats (Capra hircus) from the Laguna region in the State of Coahuila, Mexico (latitude, 26°23'N and longitude, 104°47'W). In females isolated from males, nonbreeding season lasts from March to August and from January to April in bucks isolated from females [25], [26]. All females of the present study had given birth between August and September and were milked manually once daily during the study. Females and males were
Experiment 1—Response of females to the male effect: ovulatory activity
More than 89% of females exposed to the sexually active bucks ovulated throughout the experiment, whereas only 5% did so in the control group (P < 0.001; Table 1). Moreover, the proportions of females that ovulated were similar among groups of goats exposed for 24, 4, 2, or 1 h/d to sexually active males (P = 0.47; Table 1). However, the proportion of goats ovulating before day 4 did not differ between the control and the 1-h contact group (P = 0.23; Table 1) and this proportion was smaller
Discussion
Our results show for the first time that sexually active bucks were able to stimulate sexual activity in anovulatory goats even when the daily contact between males and females was reduced to as little as 1 h/d (experiment 1). Indeed, the ovulatory variables that we measured did not differ among groups exposed to males for 24, 4, 2, or 1 h/d at the end of the 15-d study. These results are in agreement with previous studies in which goats were either in permanent (24 h/d) or intermittent contact
Conclusion
In the present study, we showed for the first time that 1 h daily of contact between anovulatory goats and sexually active males for 15 d is sufficient to efficiently stimulate ovulatory activity. More importantly, we found that the male-induced secretion of LH differs between females exposed permanently or intermittently although the ovulatory response was similar in the long term. Indeed, our findings strongly suggest that the daily augmentations of the frequency of LH pulses resulted in
Acknowledgments
The authors are grateful to Alejandro Sandoval for providing the does used in the present study, to all members of the Centro de Investigación en Reproducción Caprina (CIRCA) of the Universidad Autónoma Agraria Antonio Narro for their technical assistance, and to Dolores Lopez for her excellent secretarial and administrative support. The authors also acknowledge Corinne Laclie and Anne Lyse Lainé from the laboratory of hormonal assay of the Station de Physiologie de la Reproduction et des
References (41)
- et al.
The physiological responses of anovulatory ewes to the introduction of rams—a review
Livest Prod Sci
(1986) - et al.
Non-pheromonal stimulation by the male of LH release in the anoestrous ewe
Physiol Behav
(1986) - et al.
Effect of male odour on LH secretion and the induction of ovulation in seasonally anoestrous goats
Anim Reprod Sci
(1990) - et al.
Lack of sexual experience does not reduce the responses of LH, estrus or fertility in anestrous goats exposed to sexually active males
Horm Behav
(2011) - et al.
The “male effect” in sheep and goats: a review of the respective roles of the two olfactory systems
Horm Behav
(2004) - et al.
The ‘male effect' in sheep and goats - Revisiting the dogmas
Behav Brain Res
(2009) - et al.
Increased plasma LH levels in seasonally anovular merino ewes following the introduction of rams
Anim Reprod Sci
(1980) - et al.
Effectiveness of testosterone-treated wethers and ewes as teasers
Appl Anim Ethol
(1982) - et al.
Male sexual behavior contributes to the maintenance of high LH pulsatility in anestrous female goats
Horm Behav
(2009) - et al.
Four hours of daily contact with sexually active males is sufficient to induce fertile ovulation in anestrous goats
Horm Behav
(2010)