Reproductive activity of Suffolk ewes in seasonal anestrus after being exposed to Saint Croix or Suffolk rams

Abstract

The purpose of this study was to examine the hypothesis that rams of a tropical breed may be more effective than rams of temperate breed in inducing a reproductive response in ewes of temperate origin during the anoestrous period. Thirty Suffolk ewes in seasonal anestrus were assigned to one of three groups. In the control group (n=9), no males were present, while in the second group (Suffolk rams [SUF]; n=9) ewes were exposed to Suffolk males continuously for 13 days and twice per day from days 14-30, while in the third (Saint croix rams [SCR]; n=12), ewes were treated as in SUF, but rams were from the Saint Croix breed. Sexual receptivity was recorded daily for 30 days after introduction of the males and lambing data were recorded in the fall in SUF and SCR groups. In addition, serum progesterone (P₄) concentration was used to monitor ovarian activity in all groups. No reproductive activity was observed in controls. In SUF, six ewes ovulated but did not show estrus, while in SCR all ewes showed estrus, ovulated and were mated. In addition, all but one of the ewes in SCR lambed. It was concluded the Saint Croix rams were more effective than Suffolk rams in inducing an estrous response, conception and pregnancy in anestrous Suffolk ewes.

Keywords:

• male effect
• Saint Croix
• Suffolk
• sexual behaviour
• seasonal reproduction

Introduction

In seasonal ruminants such as sheep, the introduction of a ram to anovulatory females previously separated from any males may induce sexual activity within a few days (Flores et al. 2002; Ungerfeld et al. 2004). This phenomenon is known as ‘the male effect’, and has been extensively studied in ewes (Martin et al. 1986).

A major limitation of the male effect is the poor reproductive response observed during the long-day photoperiod, especially in Suffolk ewes (Minton et al. 1991). Poor ewe sexual behaviour display, which limits the effect to the onset of the normal breeding season (Martin and Scaramuzzi 1983), may be due to inadequate stimulation from the male. Indeed, male behavioural and physiological activity tends to decrease during the period of female anestrus (Dufour et al. 1984; Hanif and Williams 1991).

It has been well established that high sexual activity in males enhances the female response (Perkins and Fitzgerald 1994). To increase male sexual activity, in previous studies, rams have been subjected to an artificial schedule of light and darkness that simulates a short-day photoperiod, or implanted with melatonin (Schanbacher 1988; Hanif and Williams 1991).

It is clear from the literature that the breeds that originated in temperate climates or high latitudes (>35° N) are seasonal breeders and that the annual variation in daily photoperiod is responsible for timing the annual reproductive cycle (Avdi et al. 2004). In contrast, hair sheep, which are breeds originating in the tropics, have been reported to be almost or completely a seasonal (Rosa and Bryant 2002; Aguirre et al. 2007), allowing their use as breeders during the whole year without the use of artificial light or hormone treatments.

Around the world, both tropical and temperate breeds are found at mid-latitudes (19° N). This means that it would be possible to use Saint Croix rams to induce sexual activity in Suffolk ewes. However, no studies have been conducted evaluating the possibility of a ram effect between these two breeds during the long-day photoperiod.

The present study was performed to test the hypothesis that Saint Croix rams are more effective than Suffolk rams in inducing a reproductive response in Suffolk ewes during the anoestrous period.

Materials and methods

The study was carried out at the University of the State of Morelos, Mexico, which is located at 18° 37′ N and 99° 19′ W and situated 899 m.a.s.l. The average annual rainfall in this area is of 800 mm and the average temperature is 23° C. The experiment was performed in May, which corresponds to the period of deep anestrus in the Suffolk ewe at this latitude(De Lucas-Tron et al. 1997; Arroyo et al. 2007).

Subjects

Sexually experienced Saint Croix (70.05±2.94 kg; n=2) and Suffolk (110.09±4.38 kg; n=2) four-year-old rams were used as stimuli. The animals were housed in two separate pens by breed, without visual, olfactory or auditory contact with the ewes.

In addition, 30 two-year-old multiparous Suffolk ewes weighing 80.76±0.47 kg were assigned to one of three groups: In one group Suffolk rams (SUF), nine ewes were exposed to a Suffolk male continuously for 13 days and twice per day from days 14 to 30. In other group Saint croix rams (SCR) 12 ewes were treated as in SUF, but exposed to Saint Croix rather than Suffolk rams. Control group ewes (n=9) were not exposed to rams. Each group was housed in a different pen without visual, olfactory or auditory contact among groups.

Six months before the beginning of the experiment, alimentation was standardised in all animals with ration consisting of ad libitum oat hay and 0.5 kg/animal/day of a 14% commercial concentrate (Nu3®).

Procedure

At the beginning of the experiment, one male from each breed was introduced to the housing pen (10×5 m enclosures) of the females for 24 h starting at 08:00 h. Rams from the same breed were rotated daily to avoid the negative effect of ewe and ram preferences, and to favour the novelty of the male as stimulus. From day 14 to the end of the experiment (day 30), estrous activity in response to teasing was checked daily at 08:00–08:30 and 20:00–20:30 by running ewes with the same rams used during the 13-day stimulation period.

At all times, males were fitted with harnesses and marking crayons that they had been previously habituated to wear, at all times.

Ewes from the SUF and SCR groups were considered to be in estrus when they were directly observed to accept a ride from a ram, or when crayon marks were found on their rumps. Receptive ewes were allowed to mate and receive one ejaculation from the respective teaser ram after their sexual receptivity was recorded. In addition, lambing data were recorded in the fall.

Blood samples

To assess ovarian activity, blood samples were collected from all ewes in all groups, by jugular venipuncture in vacutainer tubes on days: −8, −2, 8, 13, 23 and 29 from ram introduction. Samples were taken at 07:30, were centrifuged within the first hour after collection at room temperature (Pulido et al. 1991) and the serum remained frozen at −20°C until analysis of progesterone (P₄) concentration.

Ewes were diagnosed as seasonally anovular if the first two samples showed < 1 ng/mL of P₄ concentration. This condition was evident in all the experimental animals, except three ewes in SUF. According to Yuthasastrakosol et al. (1975), the persistence of levels < 1 ng/mL of circulating P₄ indicated the absence of functional corpora lutea.

Serum P₄ concentration was analysed by Radioimmunoanalysis (Fitzgerald and Butler 1982) at the end of the experiment. Inter-assay coefficient of variation (CV) was 8% and intra-assay CV was 12%.

Statistical analysis

The ratio of ewes among groups that displayed estrus, high levels of P₄ (>1 ng/mL) at day 8, 13, 23 or 29 and lambed after 13 days of treatment, were compared by a Proportion test (Altman 1997).

Experimental units in SUF were reduced to six because of three ewes that retrospectively were found to have concentrations of P₄ above 1 ng/mL in samples from days −8 to −2, and were not considered in the analysis, since they were cycling before subjected to treatment.

Results and discussion

No reproductive activity was observed in the control group. In SUF, three females had elevated P₄ concentrations before and after male introduction and showed estrus during the period of male exposure; these ewes were mated by the stimulus rams and lambed. The rest of the SUF group (100% n=6) ovulated after the introduction of the males but did not display estrus. In SCR all ewes showed ovarian and sexual activity after male exposure, clustering 91.66% of their estrous behaviour between days 18–22 and 25–26 (Figure 1). In addition, all but one of the ewes in SCR (91.66%) were mated and lambed.

Figure 1.  Experimental design and reproductive response of Suffolk ewes in seasonal anestrus to Saint Croix and Suffolk rams.

All ewes in the treated groups presented P₄ levels above 1 ng/mL by day 29 of the experiment. However, 77.77% (7/9) and 75% (9/12) in SUF and SCR, respectively (P>0.05), had a functional CL since day 13 (Figure 1).

The results from the present experiment showed that Saint Croix rams were more effective than Suffolk rams in stimulating sexual behaviour in Suffolk ewes during their deep anestrus period. This can be explained by breed differences, since tropical rams are not affected by long days whereas rams from breeds originated in temperate zones are in a restricted reproductive condition at this time of the year (Dufour et al. 1984; Hanif and Williams 1991; Rosa and Bryant 2002).

In a similar experiment, conducted by Tervit and Peterson (1978), they conclude that Romney ewes which is a seasonal breed, showed their first estrus earlier after being exposed to Dorset rams, which is a less seasonal breed, than those exposed to Romney rams, even though the later had higher testosterone levels. However, according to our results, less seasonal breeds might induce sexual activity in anestrus ewes due to a more intense reproductive behaviour, regardless of testosterone concentration.

At mid latitudes (19° N), the Saint Croix, which is a tropical (Caribbean) hair breed, is sexually active throughout the year (Fitzhugh and Bradford 1983), whereas the Suffolk has a restricted reproductive season (De Lucas-Tron et al. 1997). Unlike wooled sheep that have evolved in temperate regions, hair sheep show no evidence of a photoperiodic effect on fertility at tropical latitudes (Fitzhugh and Bradford 1983). Furthermore, Godfrey et al. (1988) observed that, under tropical conditions, Saint Croix rams display full reproductive activity during the month of June.

The fact that most of the ewes had P₄ levels above 1 ng/mL by the end of the continuous male exposure period (day 13), is in accordance with Chemineau et al. (2006), who found that females ovulate within three days after the introduction of males. However, this ovulation is usually not accompanied with estrus signs (Schinkel 1954).

According to Martin et al. (1986), ewes show two peaks of estrus after ram exposure, one at 17–20 days and one at 21–25 days after exposure. In the present study, ewes exposed to Saint Croix males showed a similar exhibition of estrous symptoms.

In the group exposed to Suffolk rams, however, even though some ovarian activity was observed no ewes displayed estrus except the three ewes that were already cycling. In the other six ewes, the intensity of the stimulus exerted by the Suffolk rams was probably strong enough to induce ovulation but not to induce estrous behaviour (receptivity), although three estrous females were present in this group and could have interacted with the male, forming a sexual active group and enhancing the response of the six anestrous ewes.

The Suffolk breed has marked reproductive seasonality even at 19° N (De Lucas-Tron et al. 1997). It is, therefore, difficult to explain why three ewes in group SUF were cycling before male introduction even though they were in the deepest part (May) of the anestrus season. However, Thimonier and Mauléon (1969) mentioned that in some breeds a certain proportion of the ewes do not interrupt their reproductive activity, which means they are able to show spontaneous ovulation during the anestrus.

Signoret et al. (1982) determined that 20% of ewes ovulated when exposed to teasers for 24 h, and that this percent is increased to 51% after four days of exposure and to 61% after 13 days of exposure. In the present experiment the latter percentage was 100% when using Saint Croix rams.

Conclusion

It seems fair to conclude that Saint Croix rams induced a greater reproductive response in anestrous Suffolk ewes than Suffolk rams, inducing a greater estrous response, conception and pregnancy rate, in part, perhaps explained by differences in the amount of courtship behaviour displayed by both breeds. Although, it is unclear whether this is a result of the increased ram sexual behaviour alone or its combination with production of pheromones, other audio-visual signals (Delgadillo et al. 2009) or testosterone levels (Tervit and Peterson 1978). More studies are needed to understand how this effect works.

Implications

Nowadays, sheep breeders from all over the world are searching for ways to increase the efficiency of sheep farming. The use of Saint Croix rams to induce a male effect in Suffolk ewes at mid latitudes appears to be an effective method for achieving this goal. Furthermore, teaser Saint Croix rams could be used to induce sexual activity in Suffolk ewes, thus, allowing insemination by Suffolk rams.