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Effect of season on the resumption of postpartum cyclic

ovarian activity in Mou¯on (

Ovis gmelini musimon

)

and Manchega sheep (

Ovis aries

)

J. Santiago-Moreno

*

, A. GonzaÂlez de Bulnes,

A. GoÂmez Brunet, A. LoÂpez SebastiaÂn

Departamento de ReproduccioÂn Animal y ConservacioÂn de Recursos ZoogeneÂticos, SGIT/INIA, Avda. Puerta de Hierro s/n, 28040-Madrid, Spain

Accepted 29 July 1999

Abstract

The objective of this study was to compare ovulatory activity of Mou¯on and Manchega ewes lambing at different times of the year. A total of 38 adult European Mou¯on and 26 Manchega ewes were divided into two groups according to whether lambing occurred in late winter/early spring or summer. Plasma progesterone concentrations were monitored to assess the interval to ®rst ovulation after parturition. Both season and type of sheep affected the postpartum interval. When parturition occurred towards the end of the breeding season for Mou¯on (February±March), 12 of 26 animals had a mean (s.e.) interval to ®rst ovulation of 251.8 days and exhibited between 1 and 6 short or normal cycles before the onset of anoestrus. The remaining 14 animals did not resume ovulatory activity until the following breeding season which started in October. Similarly, female Mou¯on (nˆ12) giving birth in June reinitiated their breeding activity only at the start of the following season in October. Manchega ewes that lambed in April (nˆ11) and June (nˆ15) had postpartum intervals to ®rst ovulation of 111.54.1 and 31.51.9 days, respectively. Both groups of Manchegas reinitiated ovulatory activity at the start of the expected breeding season for the breed (July). It can be concluded that the time of year is a major factor controlling the duration of ovarian inactivity following parturition in both Mou¯on and Manchega ewes.#2000 Elsevier Science B.V. All rights reserved.

Keywords:Mou¯on; Manchega sheep; Ovulation; Postpartum

1. Introduction

In sheep, the interval between parturition and the resumption of ovarian activity has been shown to be

in¯uenced by numerous factors such as suckling intensity (Schirar et al., 1989a), season of parturition (Pope et al., 1989; Delgadillo et al., 1998), uterine involution (Schirar et al., 1989b), management of the ¯ock, body condition and nutrition (Pope et al., 1989; Mbayahaga et al., 1998). Among these factors, the date of lambing is to a large extent determined by seasonal effects in most sheep from temperate areas. If *Corresponding author. Tel.: ‡34-1-3474022; fax:

‡34-1-5490956.

E-mail address: moreno@inia.es (J. Santiago-Moreno).

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lambing occurs towards the end of the reproductive period, the postpartum anoestrus will overlap with the seasonal anoestrus (Fitzgerald and Cunningham, 1981). However, when lambing occurs at the height of the breeding season, cyclical ovulatory activity can be resumed within 30 days postpartum (Amir and Gacitua, 1987). Consequently, the duration of the interval between parturition and the resumption of reproductive activity will determine the frequency of lambings and the overall lifetime productivity of the sheep.

Although normal ovarian cyclic activity after lamb-ing is often preceded by one or more short cycles and silent ovulations (Quirke et al., 1983; Mbayahaga et al., 1998), these are believed to be necessary prerequisites for estrous behaviour (Schirar et al., 1989a; Goodman, 1994). However, there are large breed differences on the extent of the postpartum anoestrus prior to a fertile oestrus, re¯ecting a strong genetic component in addition to seasonal in¯uences (Pope et al., 1989).

The Manchega sheep is a domesticated Spanish breed that exhibits a long breeding season from June±July until February±March (GoÂmez-Brunet and LoÂpez-SebastiaÂn, 1991). At the other extreme, the European Mou¯on (Ovis gmelini musimon) is a primitive sheep, originated from the Mediterranean area, that exhibits a shorter breeding season (Hafez, 1952), ranging from October to February±May (San-tiago-Moreno et al., 1995). However, in comparison with most breeds of domestic sheep, the duration of their postpartum anoestrus has not been precisely estimated by progesterone measurement.

Given the close genetic relationship between Mou-¯on and domestic sheep (Wang et al., 1991) and their distinct breeding seasons, the objective of this study was to determine the genotypic differences in the interval from parturition to the ®rst ovulation and how this interacts with the effect of season. Further-more, the knowledge of the postpartum anoestrus periods in the wild sheep could be useful for improv-ing the reproductive management practices in farmed Mou¯on herds.

2. Material and methods

Two groups of mature Mou¯on (nˆ38) and Man-chega (nˆ26) ewes were kept at the facilities of the ``Animal Reproduction Department-INIA, Madrid

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3. Results

There was a signi®cant (P< 0.001) effect of time of parturition on the duration of the interval between lambing to ®rst ovulation in both Mou¯on and Man-chega sheep. Of the 26 female Mou¯on that lambed in the February±April period, 12 had an average interval between parturition and ®rst day of occurrence of ovulation of 251.8 days (Table 1). These animals exhibited between 1 and 6 cycles (mean 2.70.3) between March and June, which were quite variable in duration (Table 1) and plasma progesterone pro®les (Fig. 1). It was also observed that there were more cycles in those animals lambing earlier in the period February±April. These cycles were followed by a mean anovulatory period of 147.65.3 days until cyclical activity was resumed in October. In the remaining 14 Mou¯on which lambed in the Febru-ary±April period, ovulatory activity was absent until the next breeding season (Fig. 1).

In the Mou¯on ewes lambing in the June±July period (nˆ12), the mean interval from parturition to the ®rst ovulation was 116.76.1 days, with cyclic activity resuming in October (Fig. 2).

In Manchega ewes, the mean interval between parturition and ®rst ovulation for the 11 animals which lambed in April was 111.54.1 days and ranged between 30 June and 17 August, coinciding with the start of the breeding season. The duration of oestrous cycles and plasma progesterone concentration pro®les of the ®rst cycle presented signi®cant individual var-iations (Fig. 3). For ewes lambing in June (nˆ15), the mean postpartum interval was 31.51.9 days (Fig. 3), thus coinciding with the beginning of the breeding season for Manchegas.

The number of Mou¯on and Manchega ewes pre-senting cycles of short duration is given in Table 1. When lambings occurred towards the end of the

Table 1

Mean (s.e.) postpartum interval to the date of ®rst ovulation in Mou¯on (nˆ38) and Manchega ewes (nˆ26) and number of animals showing cycles of8, 10±14 and 15±18 days (a and b are signi®cantly different atP< 0.05)

Group Parturition in late winter/early spring Parturition in summer

Days from lambing

No. of ewes

Animals showing cycles of: Days from lambing

No. of ewes

Animals showing cycles of:

8 (days)

10±14 (days)

15±18 (days)

8 (days)

10±14 (days)

15±18 (days)

Mouflon 25.0a1.8 12 3 3 6 116.76.1 12 1 2 9

201.82.6 14 0 0 14

Manchega 111.54.1 11 0 4 7 31.5b1.9 15 2 0 13

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breeding season for Mou¯on and start of breeding season for Manchega, the number of short cycles (<15 days) were greater (P< 0.05) in Mou¯ons than Man-chega ewes.

4. Discussion

The results of the present study demonstrate that the duration of postpartum anoestrus in both Mou¯on and Manchega ewes is strongly in¯uenced by the time of the year when parturition occurs. The postpartum interval to ®rst ovulation was approximately one month in both types of sheep when parturition occurred in the breeding season. When females gave birth outside of their respective reproductive seasons, breeding activity only began again at the onset of the following breeding season.

Of particular interest was the observation that resumption of postpartum ovarian activity was not resumed until the beginning of the following breeding season in 14 of 26 Mou¯on which lambed in Febru-ary±April, within the period considered to be the end of breeding season of Mou¯on, re¯ecting an overlap of the postpartum and seasonal anoestrus. Possibly, these Mou¯ons lambed towards the onset of their seasonal anoestrus, since it has been showed that the cessation of the breeding season in Mou¯ons is very variable, ranging from February to May (San-tiago-Moreno et al., 1995). Other factors that can in¯uence the duration of the postpartum anovulatory period are body condition at lambing (Robinson, 1996) and suckling (Fitzgerald and Cunningham, 1981). Poor body condition at the time of parturition and the suckling stimulus has been shown to delay the return of reproductive activity in other primitive sheep (Bunnell and Olsen, 1981; Festa-Bianchet, 1988). Although all Mou¯ons apparently showed a correct nutritional state under the captivity conditions, the body condition was not systematically controlled, so its effect on the delay of the resumption of postpartum cyclic ovarian activity, in some Mou¯ons, cannot be categorically eliminated. A greater milking and suckling stimuli, since lambs were in continuous contact with their dams and some Mou¯ons may have suckled two or more lambs, may in¯uence the resumption of ovulatory activity. A similar behaviour has also been observed under wild conditions, with

Fig. 2. Progesterone (P4) pro®les of three Mou¯on ewes after the June±July lambing: resumption of postpartum cyclical activity occurred in October coinciding with the onset of the breeding season.

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female Mou¯ons suckling lambs of other dams (see Pfeffer, 1967).

In Mou¯on and Manchega ewes lambed in their breeding season, the period of postpartum quiescence is similar to that shown by well-fed suckling ewes of various breeds (Schirar et al., 1989a; Mandiki et al., 1990; Rubianes et al., 1996). Although the mean interval from lambing to ®rst ovulation was shorter in Mou¯on than in Manchega ewes, this slight differ-ence may be attributed to the differdiffer-ence in the timing of lambing: the end of the breeding period in Mou¯on (February±April) and the beginning of the same period in Manchega (June±July). The presence of ovarian cyclicity in these 12 Mou¯ons in late winter/early spring has not been observed in other wild sheep and suggests that the European Mou¯on is the only wild breed capable of lambing twice in the same year. Indeed, some ®eld observations revealed that breeding activity and successful conception occurred in 3 of 15 Mou¯ons from April to June (Bottorff, 1975). Although Pfeffer (1967) suggested that Mou¯on ewes lambing in the spring were those that lost their lambs from the previous mating in autumn, other studies indicate that female Mou¯on with suckling lambs may become pregnant at the spring mating (Bottorff, 1975). However, ovulatory activity in early postpartum could not be always associated with successful conception and parturition (LoÂpez SebastiaÂn and Inskeep, 1988; Hamadeh et al., 1996).

In the current study, the incidence of short cycles preceding normal ovulatory cyclic activity after lamb-ing differed between groups. When lamblamb-ing occurred within the breeding season, short cycles were more frequent in the wild breed. The difference in the timing of lambing, the end of the breeding period in Mou¯on ewes and the beginning of the same period in Man-chega sheep, may have a decisive effect on these variations. Wallace et al. (1992) reported that impaired luteal function in sheep lambing within the reproduc-tive period was more frequent at day 21 postpartum than at day 35 postpartum. Earlier resumption of postpartum ovulatory activity in Mou¯on ewes may also be responsible for the greater frequency of short cycles. In fact, between 1 and 6 ovulations occurred in these Mou¯on ewes after parturition, re¯ecting a high variability among individuals. Many of these cycles were of short duration, suggesting that an inadequate follicular development before ovulation may have

resulted in a poor luteal function. This situation may be comparable to that of the seasonally anoestrus ewe, in which a single injection of Gn-RH will induce ovulation, but the resultant corpus luteum fails to secrete normal levels of progesterone (McLeod and Haresign, 1984). Similarly, when seasonally anovula-tory ewes are induced to ovulate by the ram effect, in a variable proportion of the ewes (usually around 50% in Merinos), the corpus luteum appear to age far more rapidly and within 5±6 days of ovulation they are already involuted (Martin et al., 1986). In the present study, the number of postpartum luteal phases in some Mou¯on may have been in¯uenced by the suckling stimulus since lambs were in continuous contact with their dams and some ewes may have suckled two or more lambs. Nevertheless, although lactation has been found to cause small delays (6 days) in the resump-tion of normal oestrous cycle, it is believed to act as a protective mechanism ensuring a harmonious post-partum ovarian activity (Schirar et al., 1989a).

Females giving birth outside of their respective reproductive seasons, breeding activity only began again at the onset of the following breeding season, which is consistent with reports for other breeds (Amir and Gacitua, 1987). In Mou¯on and Manchega ewes whose postpartum anoestrus and seasonal anoestrus overlapped, no interspeci®c differences were observed in the incidence of luteal phases of short duration.

5. Conclusion

These results clearly demonstrate that season of parturition is the ®rst limiting factor on the resumption of postpartum ovarian cyclicity, which is in¯uenced by breed differences in the seasonal rhythm of reproduc-tive activity. This effect was expressed as a complete cessation of ovarian cyclicity when parturition took place within the anoestrus period. However, when ewes lambed within the breeding season, resumption of ovarian cyclicity occurred at approximately one month postpartum in both Manchega and Mou¯on ewes.

Acknowledgements

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com-ments and assistance on the preparation of the manu-script. This work was supported by DGICYT grant PB-435.

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