Directory UMM :Data Elmu:jurnal:S:Small Ruminant Research:Vol37.Issue1-2.Jul2000:

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Monitoring of estrous cycle of ewes by

ram-seeking behavior

R. Ortman

*

Department of Biology, City College of New York, New York, NY 10031, USA

Accepted 6 December 1999

Abstract

For 6 years adult, non-synchronized Hampshire ewes (n2, 5, 8, 8, 9 and 12) and rams (n6, 10, 12, 11, 11 and 9) were maintained separately and released to contiguous pastures having in common a woven-wire fence about 80 m long and 1.1 m high. Natural estrous cycles were monitored daily by observations of ram-seeking behavior as de®ned as a ewe being persistent in staying at the common fence with attention focused on the ram to the virtual exclusion of grazing. Day 0 of the estrous cycle is the ®rst day that ram-seeking is observed. One hundred and thirty four fence stays and 115 estrous cycles have been observed. For cycles falling within the normal range, the mean cycle duration (SE) was 16.530.03 days. During the ®rst four study years, a copulation test with an intact ram, carried out on a spot-check basis, indicated that all tested ewes showing ram-seeking, except one, were in estrus. Ram-seeking never occurred outside of the estrous period of the cycle. During the ®fth year, daily copulation tests with an intact ram and daily observations for ram-seeking has indicated that estrus generally lasts about two days while ram-seeking lasts for one of these days, so that the two behaviors while overlapping are not coextensive. During the sixth year, daily copulation tests with a vasectomized ram showed again a partial coincidence of the two behaviors, but also that occasionally they appeared to have the same duration. It is concluded that the utilization of ram-seeking provides an alternative, practical means to monitor the estrous cycle.#2000 Elsevier Science B.V. All rights reserved.

Keywords:Ram-seeking; Hampshire sheep; Estrous cycle; Copulation test; Cycle duration

1. Introduction

The search for the ram and movement toward him, shown only by the ewe in estrus, has been referred to as ram-seeking (Hart, 1985). This behavior was men-tioned by McKenzie and Terrill (1937) and Grant (1934) with free running animals, but demonstrated

in paddocks utilizing tethered rams by Inkster (1957), Lindsay (1966), Lindsay and Fletcher (1972) and Allison and Davis (1976). However, the use of ram-seeking as a primary means of monitoring the estrous cycle apparently has never been reported (Bathaei, 1996).

The present paper describes the physical set-up in which ram-seeking occurred and presents the data obtained with its use to monitor the estrous cycle.

Small Ruminant Research 37 (2000) 73±84

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present study is remarkably similar to published means for the same breed (McKenzie and Terrill, 1937) or other breeds (Bathaei, 1996).

During the ®rst 4 years of this study, ewes that exhibited ram-seeking were checked sporadically for estrus using an intact ram. In the ®nal 2 years of this study, all ewes were observed daily for ram-seeking and checked daily for estrus with an intact ram (1997) or a vasectomized ram (1998). It has been found that the abilities to show ram-seeking and estrus overlap temporally, but are not necessarily coextensive. Pre-liminary ®ndings were reported earlier (Ortman, 1995).

2. Materials and methods

2.1. Animals and pastures

Adult Hampshire sheep were maintained in uni-sexual groups consisting of 2±12 ewes and 6±12 rams depending on the year in question (Tables 1, 2 and 3) in separate barns and released daily except on stormy days and emergencies (footnotes, Table 1) to contig-uous pastures. Rams were let out ®rst. A woven-wire fence approximately 80 m in length and 1.14 m in height separated these pastures. Visibility was unob-structed along this fence. Sheep had access to their barns during the day and were con®ned to the barn after dark at which time they were given hay and sheep pellets (Agway). Water and mineral mix were supplied ad libitum.

Each ewe was marked with a highly visible colored spot (6±9 cm diameter) with stock marker (Donaghys) placed in a unique location so that a ewe could be identi®ed at a distance and in dim light (using bino-culars, if necessary).

2.2. Ram-seeking behavior

Since the onset of ram-seeking behavior, as well as its ®nal display, can take place at any time, observa-tions on ram-seeking were carried out intermittently throughout each day. A ewe that separates herself from other ewes by coming to, and staying at, the common fence with her attention focused on the rams on the opposite side, to the virtual exclusion of grazing while at the fence, was considered showing ram-seeking

(Figs. 1 and 2) (Hecker, 1983). The stay at the fence can be relatively continuous or discontinuous with brief intervals of absence from the fence for grazing. The span of time from the ®rst observation of ram-seeking until its terminal display or until the enclosure of the ewe, whichever came ®rst, has varied from about 0.5±11.5 h. Ewes showing ram-seeking for 1 h or more have been scored R (Table 1) or(Tables 2 and 3). Those few ewes exhibiting ram-seeking for about 0.5 h have been scored (RB [Table 1] or B [Tables 2 and 3]). Ewes who made a momentary stop at the fence while enroute to a grazing location were not included. Finally, ewes considered as showing ram-seeking must be close to the fence, so that the distance of separation between the ewe's side and the fencing was less than her width (Fig. 2), or that her rostral end made contact with the fencing at some point during her stay.

The ®rst day that ram-seeking was exhibited was considered as Day 0 of the estrous cycle; the cycle length is from Day 0 until the next day 0 (Hecker, 1983).

2.3. Copulatory test

To con®rm estrus in displaying ewes on a spot-check basis during the ®rst 4 years of this study (Table 1) they were captured at the fence, placed in a mating room, and introduced to an intact ram. If the ram mounted and began shallow thrusting movements (Bermant et al., 1969), a ewe was considered to be in estrus. If the ram failed to initiate sexual activity (a rare event), he was replaced. In general, the copulating pair was left together overnight. If the ewe was not in estrus, the animals were promptly returned to their respective groups. During the ®fth year (Table 2), copulatory tests with an intact ram were given daily to all ewes after they were secluded for the night. If a ewe was in estrus, several copulatory sequences were permitted. During the ®nal year, copulatory tests were carried out with a vasectomized ram after enclosure (Table 3).

3. Results

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anticipa-Table 1

Dates of ram-seeking (R), test of sexual receptivity (C) to intact ram and parturition (Pa) in Hampshire sheepa

Year (a) and group size

No. 34 b: 2/2/86

No. 33 b: 27/1/86

No.65 b: 18/3/93

No. 62 b: 2/5/92

No. 47 b: 10/4/90

No. 72 b: 19/2/95

No. 71 b: 30/4/94

No. 69 b: 24/4/94

No. 73 b: 3/3/95

1992 12/l0 R 3/9 R ± ± ± ± ± ± ±

2 E (b) 28/11 RC 20/9 R

6 R (b) 22/4/93 Pa _{7/10 R} 25/10 RC 18/3/93 Pa

1994 18/9 R 25/9 RC 30/9 RC 27/10 RC NR ± ± ± ±

5 E 6/10 RC 19/2/95 Pa

l0 R 3/3/95 Pa

1995 (c) 1/10 RE 7/10 R 29/10 RE 7/11 R 20/11 RC 13/10 R 30/11 RO NR ±

8 E 18/l0 R 24/l0 RC 14/4/96 Pa _{29/10 R}

12 R 5/11 R 19/3/96 Pa 14/11 R

21/11 RC 30/11 R

17/4/96 Pa

1996 (d) Ex (e) 21/9 R 31/10 R 22/10 RE 21/10 R 13/11 R 5/11 R 30/10 RB 18/10 R

8 E 8/10 R 16/11 R 10/12 RC 6/11 RC 30/11 RBC 20/11 RO 16/11 RC 7/12 RBC

11 R 25/10 R 2/12 RC 3/4/97 Pa _{23/4/97 P}a _{7/12 RO} _{14/4/97 P}a _{7/5/97 P}a

11/11 RE 29/11 R(f)

a_{Rewe displays ram-seeking (no test of sexual receptivity done); RBewe displays ram-seeking brie¯y; Cewe in standing heat to intact ram; O}_{ewe not in standing heat;}

NRno ram-seeking observed; ±ewe not born or not included; REram-see king extended into a second day; Paparturition; (a) no tests carried out in 1993; (b) Eewe, Rram; (c) testing period 1/10±30/11; 29% of days no test; (d) testing period 21/9±21/12; 13% of days no test; (e) excluded (Ex) for reason of decrepitude; (f) not given test for sexual receptivity because of her age.

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Table 2

Daily testing of ewes for ram-seeking (R) and sexual receptivity (C) to intact rama

Year and group size

Ewe No. 62 65 69 71 72 73 74 75 81

Birth date 2/5/92 18/3/93 24/4/94 30/4/94 19/2/95 3/3/95 19/3/96 19/3/96 14/4/96

1997 Test date R C R C R C R C R C R C R C R C R C

9 E 19/9 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

11 R 22/9 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ p ÿ ÿ

23/9 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

25/9±30/9a ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

1/10 ÿ ÿ ÿ ÿ B ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

3/10 ÿ ÿ ÿ ÿ P ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

4/10 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

5/10 B ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

6/10 ÿ ÿ ÿ ÿ ÿ B ÿ ÿ ÿ ÿ ÿ ÿ

7/10 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

8/10 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

9/10 ÿ ÿ ÿ ÿ ÿ ÿ ÿ

10/10 ÿ ÿ ÿ ÿ P ÿ ÿ ÿ P ÿ

11/10±20/10a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _P _P

21/10 ÿ ÿ ÿ ÿ ÿ

22/10 B ÿ ÿ

23/10 NT ÿ NT ÿ NT

24/10 ÿ ÿ P

25/10 ÿ ÿ ÿ

26/10±5/11 ÿ ÿ ÿ ÿ

6/11 ÿ ÿ ÿ

7/11 B ÿ ÿ

8/11 ÿ ÿ ÿ ÿ

9/11 ÿ ÿ

10/11 ÿ ÿ ÿ

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11/11±21/11a _ÿ _ÿ _ÿ _ÿ

22/11 ÿ ÿ

23/11 ÿ ÿ ÿ

24/11 ÿ ÿ

25/11 ÿ ÿ

26/11±30/11a _ÿ _ÿ _ÿ _ÿ

4/12 ÿ ÿ ÿ ÿ

7/12 ÿ ÿ ÿ ÿ

8/12 B ÿ ÿ

10/12 ÿ ÿ ÿ ÿ

12/12 ÿ ÿ B

Date of parturition (1998)

± ± 25/2 3/3 16/3 5/3 3/3 13/2 5/3

a_{Ppregnant; Cexhibits standing heat; Cÿdoes not exhibit standing heat; Rshows ram-seeking; Rÿdoes not show ram-seeking; RBshows ram-seeking brie¯y;}

NTno test;a_{dates inclusive.}

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Table 3

Daily observation of ewes for ram-seeking (R) with testing of ewes for sexual receptivity (C) to vasectomized ram during period 16/11 through 27/12

Year and group size

Ewe 47 62 65 71 72 73 74 75 81 84 87 88

Birth date 10/4/90 2/5/92 18/3/93 30/4/94 19/2/95 3/3/95 19/3/96 19/3/96 14/4/96 14/4/97 23/4/97 28/4/97 Test date

R C R C R C R C R C R C R C R C R C R C R C R C Note

1998 29/8 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

12 E 30/8 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

9 R 31/8±2/9a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

3/9 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

4/9±10/9a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

15/9±17/9a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

21/9±27/9a ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

1/10±3/10a ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

5/10 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

8/10±10/10a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

11/10 NT

14/10 NT

21/10 ÿ ÿ ÿ ÿ B ÿ ÿ ÿ ÿ ÿ

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23/10±27/10a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

28/10 NT

31/10b _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

1/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ P ÿ

6/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

7/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

9/11 NT

11/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ B ÿ ÿ

12/11±15/11a ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

16/11c ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

19/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

21/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

22/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

23/11 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

26/11 NT

29/11±1/12a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

7/12 ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ ÿ

8/12±9/12 NT

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Table 3 (Continued)

Year and group size

Ewe 47 62 65 71 72 73 74 75 81 84 87 88

Birth date 10/4/90 2/5/92 18/3/93 30/4/94 19/2/95 3/3/95 19/3/96 19/3/96 14/4/96 14/4/97 23/4/97 28/4/97 Test date

R C R C R C R C R C R C R C R C R C R C R C R C Note

13/12±19/12a _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ _ÿ

22/12±23/12 NT

Date of parturition

N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A 25/3/99 N/A

a_{Dates inclusive.}

b_{Intact ram used selectively on 4/10 and 31/10.}

c_{Vasectomized ram used exclusively 16/11 through 27/12; Rshows ram-seeking; RBshows ram-seeking brie¯y; Rÿdoes not show ram-seeking; Cexhibits standing}

heat; Cÿdoes not exhibit standing heat; Ppregnant; NTno tests on date.

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Fig. 1. Ewe No. 65 exhibiting ram-seeking by standing parallel to the fence. Two rams are on the opposite side.

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tion of the arrival of the ewes. However, on most days, the ewes, after leaving their barn, commenced to graze and did not come to the common fence.

On an occasional day during the breeding season, a single ewe (rarely two ewes) came to, and stayed at, the common fence (Fig. 1). Such a ewe that has separated herself from the ewe ¯ock was considered as displaying ram-seeking behavior. Typically, the ewe oriented herself parallel to the fence with her head turned toward the rams but she continued to shift her locus along the fence and to alternate the side of her body next to the fence. Ewes have been observed to stay at the fence from 0.5±11.5 h; during this time, they did not graze. The dates on which ram-seeking was shown and the results of the copulatory tests are presented in Tables 1, 2 and 3 along with the birth dates of the ewes and the group size for each year of the study. Ram-seeking was closely linked to estrus. When ewes showing ram-seeking were tested, on a spot-check basis, for estrus, they always exhibited standing heat except for No. 71, which was consistently not in estrus (Table 1).

When ewes were tested daily for both ram-seeking and estrus, it was found that ram-seeking was shown only by ewes that were also in estrus (Table 2) except for No. 71, which generally showed only ram-seeking. No. 81 was unusual in that she did not show ram-seeking, yet she exhibited estrus (Table 2). However, in the next breeding season, she did show both beha-viors once (Table 3).

In general, ram-seeking lasted only one day whereas estrus lasted an additional consecutive day (Tables 2 and 3). This difference in duration of the two behaviors was found in six different ewes. In addition, three ewes showed both behavioral reactions extend-ing over 2 days. Two ewes showed the behaviors to occur on adjacent days. Gaps in surveillance make it impossible to know if the two behaviors are ever con®ned to the same day.

The frequencies of estrous cycles of different lengths are set out in Table 4. One hundred and four cycles were obtained within the normal range (14±19 days). Their mean (_{SE) was 16.53}_{0.03 days. Four}

possible double cycles and four possible triple cycles as well as two short cycles and one cycle of 22 days were also found.

After one copulation test with an intact ram, normal pregnancies were obtained from ewes No. 33, 34, 47,

69, 72, 73, 74, 75, 81 and 87. Ewes no. 62 and 65 remained barren in the 3 or 4 years, respectively that they were given copulation tests. The successful

Table 4

Frequency of estrous cycles of speci®ed length in Hampshire ewes determined by observations of ram-seeking

Cycle length (days) No. of cycles

6 1

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pregnancy of ewe No. 71 in 1997 was quite unex-pected.

The results of the investigation over 6 years are summarized in Table 5. The overall success in the copulation test was 82% with ewes showing ram-seeking and 4% with those not showing ram-ram-seeking. If the atypical ewe (No. 71) is excluded from the calculation, the percentages success in the copulation test is 89%. The low percentage of success with ewes not showing ram-seeking is probably accounted for by continuance of estrus into Day 1 while, in general, ram-seeking is not shown after Day 0.

The pregnancy of ewe No. 71 in 1997 was unanti-cipated since she never showed standing heat. It is presumed that the ram managed to achieve intromis-sion and ejaculation as he `rode' the ewe brie¯y while she attempted to escape. However, she did show standing heat to a vasectomized ram in the next year (Table 3).

4. Discussion

Ram-seeking and estrus were studied separately in alternate estrous cycles of synchronized ewes by Lindsay and Fletcher (1972) and in different groups of synchronized ewes by Allison and Davis (1976). Both authors reported that the incidence of ram-seek-ing was signi®cantly less than the incidence of estrus. However, at no time were the two behaviors studied in the same animal on the same day. In the present investigation, ram-seeking and estrus were found clo-sely linked so that ram-seeking occurred during a part of each estrous period. There are no observations that

cycle or outside the breeding season itself. One ewe (71) was considered abnormal since she was consis-tent in not showing estrus in testing over several years despite exhibiting ram-seeking on a number of occa-sions.

Since the capacity to show ram-seeking lasts about 1 day while estrus generally lasts into the second day, it is possible that ram-seeking is shown only while the blood titer of estrogen is highest. Lindsay and Fletcher (1972) believe that the estrogen requirement for ram-seeking is greater than that for estrus.

Since ram-seeking is closely linked to estrus, it should be possible to monitor the estrous cycle using ram-seeking exclusively. Most of the cycles obtained in this investigation (Table 4) were of normal length (14±19 days.) having a mean duration (SE) of 16.530.03 days. The ewes measured were yearlings, or older, and one lamb (in 1995). This mean compares well to the means 16.01 (n31) and 16.86 (n289) for Hampshire ewes (lambs included) tested with aproned rams (McKenzie and Terrill, 1937) and to the means 16.0±16.7 for the second through ®fth cycles of Hampshire lambs, tested with vasectomized rams (Foote et al., 1970).

Since ram-seeking takes place on pasture, its obser-vation is sensitive to disruption by very stormy weather. Daily surveillance of ram-seeking during the critical days when it might be shown (mean2 days) is required for a judgement on silent heats to be made.

Table 4 shows four possible triple cycles and four possible double cycles as well as short cycles. The triple cycle shown by No. 73 (Table 1) may be due to two silent heats in succession; the other three cycles

Table 5

Summary of results obtained with same-day testing for ram-seeking and estrus

Ewe shows ram-seeking Ewe does not exhibit ram-seeking

Copulation test

No. of trials 49 5611

(No.71)a

60 15b₃₁₈ (No. 81)

428 446

% Success in cop. test 82 4

% Success in cop. test (excluding No. 71)

89

a_{Consistently showed no estrus over 4 years.}

b_[R_{C] result occurred on previous or subsequent day.}

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No. 62 and 88 (Table 3) may be due to one silent heat; the other two cycles are problematic.

McKenzie and Terrill (1937) found that Hampshire ewes showed short cycles as well as multiple cycles, particularly double cycles. Multiple cycles were con-sidered due to silent heats. Bathaei (1996) also attrib-uted multiple cycles in Iranian Mehraban ewes to silent heats. McKenzie and Terrill suggest that the short cycles might be due to the early regression of the corpus luteum. Ram-seeking is evidently a device that will tend to increase the fecundity of the ewe.

5. Conclusion

Ram-seeking and estrous activity appear to be concurrent, although not coextensive, behaviors of non-synchronized Hampshire ewes showing natural estrous cycles. It is concluded that the observation of ram-seeking offers an alternative, practical method for the monitoring of the estrous cycle.

Acknowledgements

The author wishes to thank Professor Norman Schwartz of the Biology Department of City College for photographic consultation and Patricia Macomber for kind assistance with the photography.

References

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