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

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Abstract

Two experiments were conducted to (a) determine whether sexually active males are able to stimulate the sexual activity of anestrous female goats when duration of contact is reduced to an intermittent contact shorter than 4 daily hours and (b) compare the pattern of secretion of LH when anestrous goats are exposed either permanently or intermittently to males. In the first experiment, 4 groups of anovulatory goats were exposed to sexually active males for 24, 4, 2, or 1 h/d during 15 consecutive days, whereas control females remained isolated. More than 89% of females in the groups exposed to the sexually active bucks ovulated, whereas only 5% did so in the control group (P < 0.001). However, the proportion of females ovulating before day 4 was greater in the 2-, 4-, or 24-h contact groups than in the control, whereas it did not differ between the control group and the 1-h contact group (P = 0.02, <0.001, <0.001 and 0.23, respectively). In the second experiment, 3 groups of anovulatory goats were exposed permanently (24 h/d) or intermittently (2 h/d) to bucks during 5 d or remained isolated. We found that pulsatility of luteinizing hormone (LH) increased in the intermittent and permanent contact groups after males were introduced to females (P = 0.05); this pulsatility of LH remained elevated in the permanent-contact group, whereas it decreased in the intermittent-contact group, once the male was removed (P = 0.32 and 0.05, respectively). We conclude that 1 or 2 daily hours of contact with sexually active males is sufficient to stimulate ovulatory activity in anovulatory goats; however, ovulation is obtained through a different pattern of secretion of LH.

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)

  • M. Bedos et al.

    Sexually active bucks are able to stimulate three successive groups of females per day with a 4-hour period of contact

    Physiol Behav

    (2012)
  • J.A. Delgadillo et al.

    Evidence for an annual reproductive rhythm independent of food availability in male creole goats in subtropical northern mexico

    Theriogenology

    (1999)
  • G. Duarte et al.

    Reproductive seasonality in female goats adapted to a subtropical environment persists independently of food availability

    Domest Anim Endocrinol

    (2008)
  • O.J. Ginther et al.

    Follicular dynamics during the ovulatory season in goats

    Theriogenology

    (1994)
  • J. Simões et al.

    Assessment of luteal function by ultrasonographic appearance and measurement of corpora lutea in goats

    Anim Reprod Sci

    (2007)
  • S.W. Walkden-Brown et al.

    Seasonality in male Australian cashmere goats: long term effects of castration and testosterone or oestradiol treatment on changes in LH, FSH and prolactin concentrations, and body growth

    Small Rum Res

    (1997)
  • S.W. Walkden-Brown et al.

    The male effect in the Australian cashmere goat. 2. Role of olfactory cues from the male

    Anim Reprod Sci

    (1993)
  • J.A. Delgadillo et al.

    Male goat vocalizations stimulate the estrous behavior and LH secretion in anestrous goats that have been previously exposed to bucks

    Horm Behav

    (2012)
  • J. Vielma et al.

    Vocalizations of male goats do not stimulate neither LH secretion nor ovulation on anovulatory female goats

    Técnica Pecuaria en México

    (2008)
  • E.J. Underwood et al.

    Studies in sheep husbandry in Western Australia. V. The breeding season of Merino crossbred and British breed ewes in the agricultural districts

    J Department Agric West Aust

    (1944)
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