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Anomalies in ovarian function of peulh ewes
THERIOCENOLOGY ANOMALIES IN OVARIAN FUNCTION OF PEULH EWES
A. YENIKOYE, J. PELLETIER+, D. ANDRE+, J.C. MARIANA+
University of Niamey - Biology Department B.P. 10662, Niamey (Niger) + I.N.R.A. - Station de Physiologie de la Reproduction 37380 Nouzilly (France) Received for publication: July 22, 1981 Accepted: February 11, 1982
ABSTRACT The ovarian activity of 8 Niger Peulh ewes was followed for 2 l/2 years by assaying the levels of progesterone in blood plasma sampled daily and by endoscopic observation. Although the ewes did not experience seasonal anestrus, their cycles were not regular. Most animals had persistent corpora lutea at some stage, but particularly in June. This resulted in cycles averaging 49.9z6.8 days in length instead of the normal 16.920.1 days. Intervals between successive luteal phases lasted 4-15 days as compared with 2.320.06 days seen in normal cycles. This occurred in most ewes at least once during the period from December to April. In these cases, the preovulatory discharge of LH was delayed until 7.521.8 days after the fall in the level of progesterone. The incidence of these anomalies suggests that the ewes had 69% of the ovulations and 56% of the behavioral estrus as compared to ewes that cycled regularly.
INTRODUCTION The overall fecundity of European breeds of sheep is limited by the seasonal anestrus. In the temperate zone, ewes coannenceestrous cycles in summer and cease in spring when daylength begins to increase (1, 2, 3). Thimonier and Mauleon (I) have calculated that the non-cyclic phase occupies 51% of the year in the Prealpes breed and 69% in the Ile-de-France breed. ACKNOWLEDGEMENT: We wish to thank Dr. Mauleon and Mr. Cognie for their suggestions on the writing of this paper and Mrs. Fagu for technical assistance. Dr. Lindsay helped with the translation. This work was done in the past with the financial assistance of the International Foundation for Science (F.I.S.), Stockholm (Sweden) and l'hssociation des Universites partiellement et entierement de langue franqaise (A.U.P.E.L.F.). APRIL 1982 VOL. 17 NO. 4
355
THERIOCENOLOCY In the tropical zone, the photoperiod varies little and ewes originating from these regions are presumably capable of breeding throughout the year (4). The influence of the climate on Niger sheep is largely unknown but a preliminary study using endoscopy and analysis of plasma levels of progesterone has shown that the Peulh ewe can theoretically breed throughout the year (Yenikoye, unpubl.). However, the same study showed that reproductive activity may also be interrupted periodically by cycles with long intervals between luteal phases. In addition, a number of cycles were observed in which ewe did not exhibit estrus, despite evidence that they had ovulated, presented by elevated plasma progesterone, as well as endoscopic observation. The object of the experiment presented here was to study the importance of these reproductive problems for the reproductive potential of Niger Peulh sheep.
MATERIALS AND METHODS Animals. Eight Niger Peulh ewes, 2 to 4 years old, were observed from January 1978 to July 1980 in a field at the University of Niamey, Niger (Lat. 13.30 N, altitude 216 m). Estrus was detected twice daily at 8 h and 16 h by means of 2 rams fitted with aprons. Ewes which remained immobile while being mounted were judged to be in estrus. Exnerimental. Blood samples were taken from the jugular vein of the ewes once daily from January 1978 to December 1979 and from May 1980 to July 1980 at 7.30 h. Samples were taken 4 times per day from January to April 1980 at 8, 12, 16 and 23'h. Plasma levels of progesterone were determined by a radioimmunoassay technique ( 5), the lowest detectable level was 0.05 ng/ml with intra and interassay coefficients of variation beingIl% and 13%. LH was also measured by a radioimmunoassay technique (6). Endoscopic observations were performed on the ewes 3-4 days after estrus or, in the absence of estrus, 3-4 days after the expected time of ovulation. The number of ovulations was estimated from the number of corpora lutea (CL) visible on the ovaries. Calculation of the interval between luteal phases. At estrus, the plasma levels of progesterone are very low (O.Ol0.07 ng/ml). By averaging the results for 266 samples taken at this time, we were able to construct 95% confidence limits. We considered that values above the upper 95% confidence limit (0.2 ng/ml) corresponded to a secretion of progesterone by CL form either the preceeding or a new cycle. Using this method, we determined the length of the interval separating two luteal phases.
356
APRIL
1982 VOL. 17 NO. 4
THERIOCENOLUGY
Estimation of the effect of anomalous cycles on reproductive efficiency. We can calculate the theoretical number of cycles possible during the period of observation if all cycles were of normal length. Long luteal phases or long intervals between luteal phases mean that the actual number of cycles observed is less than this theoretical figure. To express the impact of these anomalies on reproductive efficiency, we calculated the ratio of actual to theoretical cycles during the period of observation.
RESULTS
One hundred and nine estrorlscvcles estimated to be normal averaged 16.9 + 0.1 (mean + S.E.M./ days-in length. They consisted of a luteal phase of 14.5 + 0.1 days and an interval between luteal phases of 2.3 + 0.2 days. The mean .naximumlevel of progesterone during the luteal phase was 1.8 + 0.1 ng/ml. Long luteal phases. Among the 8 ewes, 5 had at least one cycle each, ranging from 31-70 days (mean 49.9 + 6.8). Two of these ewes showed long luteal phases twice, so that there were 7 long cycles during the course of the study (Table 1). Figure 1 shows that the mean plasma levels of progesterone in these cycles (2.3 2 0.2 ng/ml) did no differ significantly from those of normal cycles. Four of the 7 cases were observed in June and the other three occurred in October, December and March. TABLE I LENGTH OF OVARIAN CYCLES IN 5 EWES WITH LONG LUTEAL PHASES
Ewe no
Length of cycle (days)
Period of year
365 365 361 361 363 362 367
69 70 32 31 42 38 67
June - August 1978 October - December 1978 June - July 1979 June - July 1980 March - April 1980 June - July 1980 December - February 1980
x + S.E.M. = 49.9 + 6.8
APRIL 1982 VOL. 17 NO. 4
357
THERIOCENOLOCY
JOURS b)
I)
JUIN
>
JUILLET
>
AOUT
v
)SEPTEMBRE
1978
Fig. 1: Plasma levels of progesterone: a) during a normal ovarian cycle, b) during a cycle with prolonged luteal activity (vertical bars represent S.E.K.). Prolonged intervals between luteal phases. Five of the eight ewes had consecutive luteal phases separated by an interval longer (4 to 15 days) than the mean between two normal oestrous cycles (2.3 2 0.06 days). Table 2 and Figure 2 show the times and durations of these abnormalities. In those animals sampled intensively between January and April, the preovulatory discharge of LH was 179 + 44 h (n=4) after the fall in levels of progesterone, compared with zl + 2 h in the same animals when their cycles were normal (Figure 3). Luteal activity also began lower than normal (151 2 5 h compared to 32 2 6 h).
358
APRIL 1982 VOL. 17 NO. 4
THERIOCENOLOGY TABLE II LENGTH OF THE INTERVAL SEPARATING TWO LUTEAL PHASES IN 5 EWES DURING THE PERIOD DECEMBER - APRIL
Ewe No
LENGTH OF INTERVAL (DAYS) ______________________~~~__~~~~_~~~~~~~__~____~~_~~~~~~~~~~ April December January February March
362
365
5 4 2 5 7
367
4
8004
12
364
5
12 2 12
4 2 1 3 4
3
4 2 4 5 4 5
8 7 I
15 10
5
3
8
I
9
4 Mean (S.E.M.) EWE no365
Dec.tnbW 79 EWE no 367
D.ccmb.r
73
JO”“Oly
79
Fcbwry79
March,9
*proI73
Hay79
Fig. 2: Plasma progesterone concentrations in five ewes showing long follicular phases. APRIL 1982 VOL. 17 NO. 4
359
THERIOGENOLOGY
Fig. 3: Plasma levels of progesterone and LH during a cycle with a long follicular phase. Climatic data. The interval between consecutive luteal phases, even when within normal limits, was not constant throughout the year but in the period from December to April it was longer than at other times (Figure 4). This can be seen to correspond to the period of largest difference between daily maximal and minimal temperature and with an overall increase in both temperature and daylength. Influence of cyclical abnormalities on the reproductive potential. Seventy eight percent of ewes which had either prolonged luteal phases or a long interval between luteal phases showed behavioral estrus. Ovulations were confirmed in 80% of cases in which the cycle was long and in 89% of cases in which the interval between luteal phases was longer than normal. In both cases, oestrus was only observed 56% of the time and ovulation 69% of the time. Only one of the eight sheep cycled regularly throughout the period of observation. All of the rest showed one or both of these abnormalities at some stage.
360
APRIL 1982 VOL. 17 NO. 4
THERIOCENOLOCY
Fig. 4: Seasonal variation in mean temperatures, photoperiod and interval between consecutive luteal phases, averaged for the years 1979 and 1980 (vertical bars indicate the S.E.M.).
DISCUSSION Our results show that the Niger Peulh sheep shows ovarian activity throughout the year but this activity is not regular. Ewes are apt to have a long luteal phase, particularly in June, and a longer than normal period between luteal phases from December to April. There was no complete anestrus comparable to that seen in sheep from temperate zones. Cyclical abnormalities such as those described here have not been recorded before in ewes,although they are common in the mare (7, 8). Both progesterone assay and endoscopy have shown that the prolonged luteal phases are the result of persistent CL which no doubt inhibit behavioural estrus as well (9, 10, 11). In the mare persistent CL are caused by insufficient uterine prostaglandin (12) and this is probably the case in the ewe. The levels of progesterone in the plasma during the prolonged luteal phase are similar to those during a normal cycle.
APRIL 1982 VOL. 17 NO. 4
361
THERIOGENOLWY
Long intervals between luteal phases were characterised by a discharge of LH an average of 7 days after the fall in progesterone. We know of no other reported examples of this phenomenon in sheep. In temperate regions seasonal sexual activity is controlled mainly by variations in photoperiod. In our case, day length varied only slightly but the pattern of Cyclical disfunction appears to be associated with changes in temperature or possibly with an interaction between temperature and photoperiod (13, 14). When considered together, the abnormalities we have observed have an important influence on the total number of cycles observed. Only 69% of the theoretical number of ovulations and 56% of the theoretical number of estrous cycles were found during the period of observation. We thus find that the Niger Peulh sheep has a potential which is hardly different from that of typical temperature-breedsheep such as Ile-de-France and Prealpes (1). Work is now proceeding to study the influence of these factors on flocks and to examine their economic importance.
362
APRIL 1982 VOL. 17 NO. 4
THERIOGENOLOCY REFERENCES 1
Thimonier J. and Mauleon P. Variations saisonnieres du comportement d'oestrus et des activites ovarienne et hypophysaire chez les ovins. Ann. Biol. anim. Bioch. Biophys. 2 (2), 233-250 (1969).
2
Dyrmundsson O.R. Studies on the breeding season of Icelandic ewes and ewe lambs. J. Agric. Sci. Camb. 90, 275-281 (1978).
3
Lax J., French L.R., Chapman A.B., Pope A.L. and Casida L.E. Length of breeding season for eight breed groups of sheep in Wisconsin. J. Anim. Sci. -49 (4), 939-942 (1979).
4
Hafez E.S.E. Studies on the breeding season and reproduction of the ewe. J. Agric. Sci. 62, 189-265 (1952).
5
Yenikoye A., Mariana J.C., Ley J.P., Jolivet E., Terqui and Lemon-Resplandy M. Modele mathematique de l'evolution de progesterone chez la vache : application et mise en evidence de difference entre races. Reprod. Nutr. Develop. -21 (4), 561-575 (1981).
6.
Pelletier J., Kann G., Dolais J. and Rosseling G. Dosages radioimmunologiques de l'hormone luteinisante plasmatique chez le mouton. Mise au point de la technique de dosage. C.R. Acad. Sci. PARIS. 266, 2291-2294 (1968).
7.
Palmer E. and Jousset B. Urinary oestrogen and plasma progestterone levels in non-pregnant mares. J. Reprod. Fert. Suppl. 3, 213-221 (1975).
a.
Stabenfeldt G.H., Hughes J.P., Evans J.W. and Neely D.P. Spontaneous prolongation of luteal activity in the mare. Equine Vet. .J*, 5 (4), 158-163 (1974).
9.
Goodman R.L. Role of ovarian steroids in the initiation and synchronization of behavioral estrus and the LH surge in the ewe. Biol. Reprod. 2, Suppl. 1, 46 A abst. (1978).
IO.
Karsch F.J., Legan S.J., Ryan K.D. and Foster D.L. Importance of estradiol and progesterone in regulating LH secretion and estrous behaviour during the sheep estrous cycle. Biol. Reprod. 3, 404-413 (1980).
11
Karsch F.J., Goodman R.L. and Legan S.J. Feedback basis of seasonal breeding: test of an hypothesis. J. Reprod. Fert. 2, 521535 (1980).
12
Stabenfeldt G.H., Neely D.P., Hughes J.P. and Kindahl H. Modification of uterine PGF 2 in domestic animals through pathologic or pharmacologic processes. 9th lntern. Congr. Anim. Reprod. and A.I. Vol. II, 27-34 Madrid (1980).
APRIL 1982VOL. 17 NO. 4
363
13
Ortavant R. Photoperiodic regulation of reproduction in the sheep management of reproduction in sheep and goats symposium 58-71. Madison Wisconsin (1977).
14
Sawyer G.J., Lindsay D.R. and Martin G.B. The influence of radiant heat load on reproduction in the Merino Ewe III duration of oestrus, cyclical oestrous activity, plasma progesterone, LH levels and fertility of ewes exposed to high temperatures before meating J. Agric. Res. 30, 1143-1162 (1979).
364
APRIL 1982 VOL. 17 NO. 4
A. YENIKOYE, J. PELLETIER+, D. ANDRE+, J.C. MARIANA+
University of Niamey - Biology Department B.P. 10662, Niamey (Niger) + I.N.R.A. - Station de Physiologie de la Reproduction 37380 Nouzilly (France) Received for publication: July 22, 1981 Accepted: February 11, 1982
ABSTRACT The ovarian activity of 8 Niger Peulh ewes was followed for 2 l/2 years by assaying the levels of progesterone in blood plasma sampled daily and by endoscopic observation. Although the ewes did not experience seasonal anestrus, their cycles were not regular. Most animals had persistent corpora lutea at some stage, but particularly in June. This resulted in cycles averaging 49.9z6.8 days in length instead of the normal 16.920.1 days. Intervals between successive luteal phases lasted 4-15 days as compared with 2.320.06 days seen in normal cycles. This occurred in most ewes at least once during the period from December to April. In these cases, the preovulatory discharge of LH was delayed until 7.521.8 days after the fall in the level of progesterone. The incidence of these anomalies suggests that the ewes had 69% of the ovulations and 56% of the behavioral estrus as compared to ewes that cycled regularly.
INTRODUCTION The overall fecundity of European breeds of sheep is limited by the seasonal anestrus. In the temperate zone, ewes coannenceestrous cycles in summer and cease in spring when daylength begins to increase (1, 2, 3). Thimonier and Mauleon (I) have calculated that the non-cyclic phase occupies 51% of the year in the Prealpes breed and 69% in the Ile-de-France breed. ACKNOWLEDGEMENT: We wish to thank Dr. Mauleon and Mr. Cognie for their suggestions on the writing of this paper and Mrs. Fagu for technical assistance. Dr. Lindsay helped with the translation. This work was done in the past with the financial assistance of the International Foundation for Science (F.I.S.), Stockholm (Sweden) and l'hssociation des Universites partiellement et entierement de langue franqaise (A.U.P.E.L.F.). APRIL 1982 VOL. 17 NO. 4
355
THERIOCENOLOCY In the tropical zone, the photoperiod varies little and ewes originating from these regions are presumably capable of breeding throughout the year (4). The influence of the climate on Niger sheep is largely unknown but a preliminary study using endoscopy and analysis of plasma levels of progesterone has shown that the Peulh ewe can theoretically breed throughout the year (Yenikoye, unpubl.). However, the same study showed that reproductive activity may also be interrupted periodically by cycles with long intervals between luteal phases. In addition, a number of cycles were observed in which ewe did not exhibit estrus, despite evidence that they had ovulated, presented by elevated plasma progesterone, as well as endoscopic observation. The object of the experiment presented here was to study the importance of these reproductive problems for the reproductive potential of Niger Peulh sheep.
MATERIALS AND METHODS Animals. Eight Niger Peulh ewes, 2 to 4 years old, were observed from January 1978 to July 1980 in a field at the University of Niamey, Niger (Lat. 13.30 N, altitude 216 m). Estrus was detected twice daily at 8 h and 16 h by means of 2 rams fitted with aprons. Ewes which remained immobile while being mounted were judged to be in estrus. Exnerimental. Blood samples were taken from the jugular vein of the ewes once daily from January 1978 to December 1979 and from May 1980 to July 1980 at 7.30 h. Samples were taken 4 times per day from January to April 1980 at 8, 12, 16 and 23'h. Plasma levels of progesterone were determined by a radioimmunoassay technique ( 5), the lowest detectable level was 0.05 ng/ml with intra and interassay coefficients of variation beingIl% and 13%. LH was also measured by a radioimmunoassay technique (6). Endoscopic observations were performed on the ewes 3-4 days after estrus or, in the absence of estrus, 3-4 days after the expected time of ovulation. The number of ovulations was estimated from the number of corpora lutea (CL) visible on the ovaries. Calculation of the interval between luteal phases. At estrus, the plasma levels of progesterone are very low (O.Ol0.07 ng/ml). By averaging the results for 266 samples taken at this time, we were able to construct 95% confidence limits. We considered that values above the upper 95% confidence limit (0.2 ng/ml) corresponded to a secretion of progesterone by CL form either the preceeding or a new cycle. Using this method, we determined the length of the interval separating two luteal phases.
356
APRIL
1982 VOL. 17 NO. 4
THERIOCENOLUGY
Estimation of the effect of anomalous cycles on reproductive efficiency. We can calculate the theoretical number of cycles possible during the period of observation if all cycles were of normal length. Long luteal phases or long intervals between luteal phases mean that the actual number of cycles observed is less than this theoretical figure. To express the impact of these anomalies on reproductive efficiency, we calculated the ratio of actual to theoretical cycles during the period of observation.
RESULTS
One hundred and nine estrorlscvcles estimated to be normal averaged 16.9 + 0.1 (mean + S.E.M./ days-in length. They consisted of a luteal phase of 14.5 + 0.1 days and an interval between luteal phases of 2.3 + 0.2 days. The mean .naximumlevel of progesterone during the luteal phase was 1.8 + 0.1 ng/ml. Long luteal phases. Among the 8 ewes, 5 had at least one cycle each, ranging from 31-70 days (mean 49.9 + 6.8). Two of these ewes showed long luteal phases twice, so that there were 7 long cycles during the course of the study (Table 1). Figure 1 shows that the mean plasma levels of progesterone in these cycles (2.3 2 0.2 ng/ml) did no differ significantly from those of normal cycles. Four of the 7 cases were observed in June and the other three occurred in October, December and March. TABLE I LENGTH OF OVARIAN CYCLES IN 5 EWES WITH LONG LUTEAL PHASES
Ewe no
Length of cycle (days)
Period of year
365 365 361 361 363 362 367
69 70 32 31 42 38 67
June - August 1978 October - December 1978 June - July 1979 June - July 1980 March - April 1980 June - July 1980 December - February 1980
x + S.E.M. = 49.9 + 6.8
APRIL 1982 VOL. 17 NO. 4
357
THERIOCENOLOCY
JOURS b)
I)
JUIN
>
JUILLET
>
AOUT
v
)SEPTEMBRE
1978
Fig. 1: Plasma levels of progesterone: a) during a normal ovarian cycle, b) during a cycle with prolonged luteal activity (vertical bars represent S.E.K.). Prolonged intervals between luteal phases. Five of the eight ewes had consecutive luteal phases separated by an interval longer (4 to 15 days) than the mean between two normal oestrous cycles (2.3 2 0.06 days). Table 2 and Figure 2 show the times and durations of these abnormalities. In those animals sampled intensively between January and April, the preovulatory discharge of LH was 179 + 44 h (n=4) after the fall in levels of progesterone, compared with zl + 2 h in the same animals when their cycles were normal (Figure 3). Luteal activity also began lower than normal (151 2 5 h compared to 32 2 6 h).
358
APRIL 1982 VOL. 17 NO. 4
THERIOCENOLOGY TABLE II LENGTH OF THE INTERVAL SEPARATING TWO LUTEAL PHASES IN 5 EWES DURING THE PERIOD DECEMBER - APRIL
Ewe No
LENGTH OF INTERVAL (DAYS) ______________________~~~__~~~~_~~~~~~~__~____~~_~~~~~~~~~~ April December January February March
362
365
5 4 2 5 7
367
4
8004
12
364
5
12 2 12
4 2 1 3 4
3
4 2 4 5 4 5
8 7 I
15 10
5
3
8
I
9
4 Mean (S.E.M.) EWE no365
Dec.tnbW 79 EWE no 367
D.ccmb.r
73
JO”“Oly
79
Fcbwry79
March,9
*proI73
Hay79
Fig. 2: Plasma progesterone concentrations in five ewes showing long follicular phases. APRIL 1982 VOL. 17 NO. 4
359
THERIOGENOLOGY
Fig. 3: Plasma levels of progesterone and LH during a cycle with a long follicular phase. Climatic data. The interval between consecutive luteal phases, even when within normal limits, was not constant throughout the year but in the period from December to April it was longer than at other times (Figure 4). This can be seen to correspond to the period of largest difference between daily maximal and minimal temperature and with an overall increase in both temperature and daylength. Influence of cyclical abnormalities on the reproductive potential. Seventy eight percent of ewes which had either prolonged luteal phases or a long interval between luteal phases showed behavioral estrus. Ovulations were confirmed in 80% of cases in which the cycle was long and in 89% of cases in which the interval between luteal phases was longer than normal. In both cases, oestrus was only observed 56% of the time and ovulation 69% of the time. Only one of the eight sheep cycled regularly throughout the period of observation. All of the rest showed one or both of these abnormalities at some stage.
360
APRIL 1982 VOL. 17 NO. 4
THERIOCENOLOCY
Fig. 4: Seasonal variation in mean temperatures, photoperiod and interval between consecutive luteal phases, averaged for the years 1979 and 1980 (vertical bars indicate the S.E.M.).
DISCUSSION Our results show that the Niger Peulh sheep shows ovarian activity throughout the year but this activity is not regular. Ewes are apt to have a long luteal phase, particularly in June, and a longer than normal period between luteal phases from December to April. There was no complete anestrus comparable to that seen in sheep from temperate zones. Cyclical abnormalities such as those described here have not been recorded before in ewes,although they are common in the mare (7, 8). Both progesterone assay and endoscopy have shown that the prolonged luteal phases are the result of persistent CL which no doubt inhibit behavioural estrus as well (9, 10, 11). In the mare persistent CL are caused by insufficient uterine prostaglandin (12) and this is probably the case in the ewe. The levels of progesterone in the plasma during the prolonged luteal phase are similar to those during a normal cycle.
APRIL 1982 VOL. 17 NO. 4
361
THERIOGENOLWY
Long intervals between luteal phases were characterised by a discharge of LH an average of 7 days after the fall in progesterone. We know of no other reported examples of this phenomenon in sheep. In temperate regions seasonal sexual activity is controlled mainly by variations in photoperiod. In our case, day length varied only slightly but the pattern of Cyclical disfunction appears to be associated with changes in temperature or possibly with an interaction between temperature and photoperiod (13, 14). When considered together, the abnormalities we have observed have an important influence on the total number of cycles observed. Only 69% of the theoretical number of ovulations and 56% of the theoretical number of estrous cycles were found during the period of observation. We thus find that the Niger Peulh sheep has a potential which is hardly different from that of typical temperature-breedsheep such as Ile-de-France and Prealpes (1). Work is now proceeding to study the influence of these factors on flocks and to examine their economic importance.
362
APRIL 1982 VOL. 17 NO. 4
THERIOGENOLOCY REFERENCES 1
Thimonier J. and Mauleon P. Variations saisonnieres du comportement d'oestrus et des activites ovarienne et hypophysaire chez les ovins. Ann. Biol. anim. Bioch. Biophys. 2 (2), 233-250 (1969).
2
Dyrmundsson O.R. Studies on the breeding season of Icelandic ewes and ewe lambs. J. Agric. Sci. Camb. 90, 275-281 (1978).
3
Lax J., French L.R., Chapman A.B., Pope A.L. and Casida L.E. Length of breeding season for eight breed groups of sheep in Wisconsin. J. Anim. Sci. -49 (4), 939-942 (1979).
4
Hafez E.S.E. Studies on the breeding season and reproduction of the ewe. J. Agric. Sci. 62, 189-265 (1952).
5
Yenikoye A., Mariana J.C., Ley J.P., Jolivet E., Terqui and Lemon-Resplandy M. Modele mathematique de l'evolution de progesterone chez la vache : application et mise en evidence de difference entre races. Reprod. Nutr. Develop. -21 (4), 561-575 (1981).
6.
Pelletier J., Kann G., Dolais J. and Rosseling G. Dosages radioimmunologiques de l'hormone luteinisante plasmatique chez le mouton. Mise au point de la technique de dosage. C.R. Acad. Sci. PARIS. 266, 2291-2294 (1968).
7.
Palmer E. and Jousset B. Urinary oestrogen and plasma progestterone levels in non-pregnant mares. J. Reprod. Fert. Suppl. 3, 213-221 (1975).
a.
Stabenfeldt G.H., Hughes J.P., Evans J.W. and Neely D.P. Spontaneous prolongation of luteal activity in the mare. Equine Vet. .J*, 5 (4), 158-163 (1974).
9.
Goodman R.L. Role of ovarian steroids in the initiation and synchronization of behavioral estrus and the LH surge in the ewe. Biol. Reprod. 2, Suppl. 1, 46 A abst. (1978).
IO.
Karsch F.J., Legan S.J., Ryan K.D. and Foster D.L. Importance of estradiol and progesterone in regulating LH secretion and estrous behaviour during the sheep estrous cycle. Biol. Reprod. 3, 404-413 (1980).
11
Karsch F.J., Goodman R.L. and Legan S.J. Feedback basis of seasonal breeding: test of an hypothesis. J. Reprod. Fert. 2, 521535 (1980).
12
Stabenfeldt G.H., Neely D.P., Hughes J.P. and Kindahl H. Modification of uterine PGF 2 in domestic animals through pathologic or pharmacologic processes. 9th lntern. Congr. Anim. Reprod. and A.I. Vol. II, 27-34 Madrid (1980).
APRIL 1982VOL. 17 NO. 4
363
13
Ortavant R. Photoperiodic regulation of reproduction in the sheep management of reproduction in sheep and goats symposium 58-71. Madison Wisconsin (1977).
14
Sawyer G.J., Lindsay D.R. and Martin G.B. The influence of radiant heat load on reproduction in the Merino Ewe III duration of oestrus, cyclical oestrous activity, plasma progesterone, LH levels and fertility of ewes exposed to high temperatures before meating J. Agric. Res. 30, 1143-1162 (1979).
364
APRIL 1982 VOL. 17 NO. 4