The effect of light environment on post-partum reproductive activity and prolactin levels in two breeds of sheep

The effect of light environment on post-partum reproductive activity and prolactin levels in two breeds of sheep

Br. vet . 7. (1985) . 141, 2 72 THE EFFECT OF LIGHT ENVIRONMENT ON POST-PARTUM REPRODUCTIVE ACTIVITY AND PROLACTIN LEVELS IN TWO BREEDS OF SHEEP P ...

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Br. vet .

7. (1985) .

141, 2 72

THE EFFECT OF LIGHT ENVIRONMENT ON POST-PARTUM REPRODUCTIVE ACTIVITY AND PROLACTIN LEVELS IN TWO BREEDS OF SHEEP P . J . PIJOAN* and H . Ll . WILLIAMS The Royal Veterinary College, Department of Animal Husbandry and Hygiene, Boitons Park, Potters Bar, Herts

SUMMARY The onset of reproductive activity in Poll Dorset and North Country Cheviot ewes, kept in local (51 ° 43'N) and in equatorial (13L :11D) light was assessed following lambing in the autumn (n = 10) and in the spring (n = 12) . The relationship between the levels of plasma and milk prolactin and the duration of post-partum anoestrus was also investigated . A clear seasonal variation in the duration of post-partum anoestrus and in the incidence of oestrus was observed in the local light environment . Ewes lambing in the autumn showed earlier and more ovarian and behavioural activity than those lambing in the spring . The mean prolactin levels in plasma and milk of ewes lambing in the local light, were significantly higher (P < 0 . 001) in the spring than in the autumn . In contrast, under equatorial light, prolactin levels did not show a significant seasonal change .

INTRODUCTION Some breeds of sheep are capable of breeding more than once a year (Hunter, 1968a and b) . To achieve a shorter lambing interval they usually conceive at a time when conditions are less than optimum for reproductive activity . In addition to post-partum anoestrus, spring lambing also coincides with the early phase of seasonal anoestrus in the majority of breeds . Seasonal anoestrum is very largely governed by changes in the photoperiod . Breeds show considerable differences in their breeding seasonality (Hafez, 1952), response to stimulation (Yeates, 1949) and dependence on fluctuating light rhythms for normal function (Williams, 1976) . The photoperiod is a major environmental factor influencing post-partum anoestrus in sheep (Mauleon & Dauzier, 1965 ; Hunter & Van Aarde, 1973 ; Sefidbakht, Mostafavi & Farid, 1977) . High levels of prolactin have been associated with anovulation during the early postpartum phase (Kann & Martinet, 1975 ; Kann, Martinet & Shirar, 1977 and 1978) . Circulating levels of prolactin also show marked seasonal variation (Thimonier, Ravault & Ortavant, 1978), thus seasonal effects must be considered when interpreting changes in prolactin levels during the post-partum period (Erb, Sitarz & Malven, 1977) . *Present address : Departamento de Reproduccion Animal, Instituto Nacional de Investigaciones Pecuarias, Apdo . Postal #41-652, Mexico, D.F ., C .P. 05110, Mexico .



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The present study was conducted to determine the onset of ovulation and oestrus after lambing and their relationship to prolactin levels in the blood and milk of two breeds, in contrasting light environments, lambing in the autumn or the spring .

MATERIALS AND METHODS Animals and treatments The ewes were maintained in the local light environment at latitude 51 °43'N or in a simulated equatorial light environment of 13L :11 D from June, 1979 . The housing and lighting has been described previously (Williams, 1976) . The autumn lambing involved five Poll Dorsets (PD) and five North Country Cheviot (NCC) ewes in each light environment . All ewes had been treated with intravaginal progestagen-impregnated sponges (Veramix, Upjohn) and 750 i .u ., PMSG (Folligon, Intervet) . All ewes lambed during the first week of October, 1980 . The spring lambing involved six ewes of each breed in each environment and lambing occurred during the first two weeks of April, 1981 . The lambs were given creep feed from their second week and weaned at approximately 11 weeks of age . Detection of oestrus Lambed ewes were exposed continuously to a vasectomized ram, fitted with harness and keeling crayon, within 24 h of lambing . In addition to twice daily inspection for keel marking, ewes were tested daily for oestrus using an unaccustomed vasectomized ram in a test pen . Behavioural observations continued for 69 days . Collection of blood samples Blood was collected by jugular venipuncture between 0900 and 1000 h with particular attention given to minimizing stress . The labelled syringes were immediately placed in ice and centrifuged within 60 min of collection at 3000 rev/min for 15 min at 4 °C . The plasma was separated and stored at -20 °C until assayed . Milk sampling was carried out following blood sampling ; 5 ml were drawn into a Bijou bottle, cooled and then frozen . Blood and milk samples were taken within 24 h of lambing and then daily until day 10 . From day 10 to day 30 sampling occurred three times/week and thereafter twice weekly until the eleventh week . Radioimmunoassays Radioimmunoassays of plasma progesterone were carried out using the conventional method of Abraham et al. (1971) as described by Gadsby et al. (1974) using an antiserum against progesterone raised in sheep (As No . P18/2), the characteristics of which have been described (Flint et al., 1978) . In this laboratory, the within and between assay coefficients of variation were 4 . 78% (n-54) and 12 . 21% (n-54), respectively, for a sample containing 1 . 88 ± 0-13 ng/ml ± SD . Mean recovery of 3 [H] progesterone was 82 . 94 ± 5 . 21% (n = 35) . Ovine plasma and milk prolactin levels were assayed by the double antibody radioimmunoassay of McNeilly & Andrews (1974) as described by Aubert (1977) . An anti-ovine prolactin serum (MCNR 2532) was used in this assay and its characteristics



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have been described (McNeilly & Andrews, 1974) . The ovine prolactin used for radioiodination was AFP-2060c and that for standards and tests was NIH-P-S 13 . The precipitating antiserum was a commercial anti-rabbit gamma globulin (donkey anti-rabbit gamma globulin RD17, Wellcome Reagents Ltd) . For any hormone, all samples from each animal were assayed together in a single assay and estimations were made in duplicate . The coefficients of variation within and between assays in this laboratory are given in Table I .

Table I Coefficients of variation within and between radioimmunoassays of plasma and milk prolactin Prolactin in sample ng/ml

n

Within assays

Between assays

Plasma prolactin 21 . 76± 5 . 29 111 . 50±27 . 86 207 . 86±41 . 45

44 40 40

7 . 76 7 . 69 7 . 04

23 . 98 24 . 68 19 . 62

Milk prolactin 28 . 01± 4 . 22 127 . 05±34 . 70 198 . 21±46 . 06

26 24 22

6 . 43 11 . 90 12 . 44

14 . 71 26 . 73 21 . 68

Determination of ovulation Ovulation was considered to have occurred when the plasma progesterone concentration exceeded 0 . 60 ng/ml on two consecutive sampling dates .

Statistical analysis Differences in prolactin levels between groups were determined by a 2X2X2X2 factorial design with breed, light environment, season, fluid (plasma or milk) and postpartum period (period 1 : day 0 to 10 ; period 2 : day 11 to 69 postpartum) as fixed effects based in least square means . Data were analysed by analysis of variance and Students' t-test .

RESULTS

Post partum reproductive activity Autumn . The number of ewes of both breeds exhibiting oestrus and ovulating, during four 17-day periods, in the two light environments, is presented in Fig . 1 . In the local light environment it is evident that all ewes of both breeds ovulated and displayed oestrus at some stage during periods 2, 3 and 4 . Oestrus was observed in only PD ewes during period 2 and this breed also showed a higher level of behavioural and ovulatory activity during period 4 .



275

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Fig. 1 . Number of ewes on oestrus (oe) and ovulating (ov) after lambing in the spring (A) or in the autumn (B), in the local and equatorial light . The shaded areas in the columns represent the number of ewes showing oestrus or ovulating for the first time . In the equatorial light environment, there were marked differences between the breeds in both criteria of activity . All PD ewes were in oestrus during periods 2 and 4 and all ewes ovulated during periods 3 and 4 . Only three of the five ewes in oestrus during period 2 showed evidence of ovulation . In NCC ewes only two ewes showed evidence of ovulation and oestrus was observed in only one ewe and not until period 4 . Spring. In contrast to the high level of reproductive activity recorded in Dorset ewes in both light environments in the autumn, the spring lambing was followed by a low level of behavioural and ovarian activity . In PD ewes oestrus was observed in one ewe in the local light during period 3 and in one ewe in period 2 in the equatorial light . Oestrus was observed in only one NCC ewe during period 3 in the local light . No oestrous periods were observed in the NCC ewes maintained in the equatorial light environment . In period 4 no oestrous periods were recorded in PD ewes in either environment and ovulation was confined to two ewes in the local light environment . The NCC ewes followed the same trend with no activity during period 4 .



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Prolactin levels in plasma and milk Plasma and milk prolactin levels from the day of parturition (day 0) up to day 61 post partum, in those ewes lambing in the local and equatorial light, during autumn 1980 and spring 1981, are presented in Figs 2 and 3 respectively . From these Figures it can be seen that in all groups of ewes, there is a marked fall in the levels of prolactin during the first 10 days after lambing . After this stage, levels tended to remain relatively constant up to day 61 when sampling was stopped . Nevertheless, it can be seen that in the local light group the basal levels found after day 10 were higher in PD and NCC ewes lambing during the spring than in those lambing in the autumn . Those lambing in equatorial light during the spring showed levels similar to the autumn-lambed ewes in the local and equatorial light. The statistical analysis of the prolactin levels in plasma and milk in these ewes, lambing under two contrasting photoperiods, in the autumn and spring, can be seen in Table II . A clear effect (P < 0 . 001) was established in the case of breed, light environment, season of lambing and period postpartum (period 1 : day 0 to 10 ; period 2 : day 11 to 61) . No significant difference was found between levels of prolactin in milk and plasma . A significant interaction (P < 0 . 001) was also established between light and season of lambing, and season of lambing and the period postpartum .

Table II Analysis of variance of prolactin levels d.f.

Source

Breed (B) Light (L) Season (S) Fluid (F) Period post-partum (PP) BXL BXS BXF BXPP LXS LXF LXPP SXPP SXPP FXPP Error *** P<0 . 001,

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 499

** P<0 . 01,

M. S.

28185 . 26*** 81943 . 29*** 362314 . 74*** 381 . 65 710828 . 55*** 2429 . 21 1068 . 18 7891 . 62* 2014 . 90 317021 . 68*** 18458 . 12** 1055 . 83 95235 . 23* 1 . 61 18272 . 41 ** 2161 . 80 * P<0 . 06 .

The mean prolactin levels found in both lambing seasons for the two breeds and light environments are presented in Table III . In the local light a significant difference (P < 0 . 001) was found in both breeds between the levels in the autumn and spring, whereas in the equatorial light no significant difference was established between the prolactin levels of the two seasons .



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Table III Prolactin levels (mean±SEM)* during two lambing seasons in Poll Dorset and North Country Cheviot ewes in local and equatorial light Poll Dorset

Autumn 1980 Spring 1981

North Country Cheviot

No .

Local

Equatorial

Local

Equatorial

5

85 . 64±9 . 26,

124 . 81±7 . 44`

82 . 57±8 . 80 1

99 . 74±8 . 521,,

6

207 . 42±8 . 506

124 . 14±7 . 42

185 . 53±8 . 42d

105 . 85±27

* Different superscripts are significantly different (P<0 . 01) . b,d>a(P<0 . 001).

DISCUSSION The marked seasonal variation in onset of reproductive activity after lambing in the local light environment is similar to that reported for a number of breeds (Hafez, 1952 ; Mauleon & Dauzier, 1965 ; Hunter & Van Aarde, 1973 ; Sefidbakht et al., 1977, and others) . This has been attributed to the dominating influence of the change in photoperiod (Hunter, 1968a) ; the beneficial effects of exposing pregnant and lactating ewes to decreasing light regimes has been demonstrated (Moseley & Lamming, 1969 ; Ducker & Bowman, 1972 ; Fraser, Gill & Robinson, 1972) . The level of activity in the springlambing Poll Dorset groups is perhaps unexpectedly low in a situation where feeding and ram management were given particular attention and where contemporaries kept unbred showed a high level of cyclic activity (Pijoan, 1982) . In the non-fluctuating equatorial light environment the performance of Poll Dorset ewes in the autumn was clearly superior to that of North Country Cheviot ewes . An earlier investigation using a similar light environment had shown differences between two other breeds in level and duration of cyclic activity (Williams, 1976) . The investigation provides further evidence of the importance of genotype-photo-environment interactions and their effects on fecundity in sheep . The difference in activity between autumn and spring-lambing Poll Dorset ewes in the equatorial light suggests that factors other than the photoperiod have an important role in the initiation of post-partum activity . The performance of unbred contemporaries indicated that the residual effect of the earlier light environment was minimal . The marked fall in `basal' prolactin levels, seen in this study during the first 10 days of lactation, has been reported previously (McNeilly, Moseley & Lamming, 1972 ; Lamming, Moseley & McNeilly, 1974) . In contrast, Kann et al. (1978) reported that in suckling ewes blood prolactin levels remained high (300 to 400 ng/ml) until 50 to 60 days postpartum. The reason for this discrepancy is not clear ; however, Prealpes ewes, which were used in Kann's experiments, are dairy ewes (Ricordeau & Denamur, 1962, cited by Ford, 1979) and that might account for an increased prolactin secretion during nursing . The seasonal variation in levels of prolactin observed in this study is similar to that reported by Erb et al. (1977) in summer and autumn-lambing ewes . Rhind et al (1980) and Fitzgerald & Cunningham (1981) have reported seasonal changes in lactating Finn and Dorset ewes . In contrast, the prolactin levels of PD and NCC ewes maintained in the



BRITISH VETERINARY JOURNAL, 141, 3

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equatorial light environment did not show a significant variation between seasons (Table III) . This gives further support to the proposition that seasonal variation in daylength is the main factor regulating seasonal variation in circulating levels of prolactin (Pelletier, 1973) . Although hyperprolactinaemia has been associated with lactational anoestrus and amenorrhoea in women (reviewed by McNeilly, 1980) and with post-partum anoestrus in sheep (Kann & Martinet, 1975 ; Kann et al., 1977 and 1978), the role of prolactin is not clear . Kann et al. (1978) have suggested that hyperprolactinaemia inhibits the positive feedback of LH and FSH to the administration of oestradiol in ovariectomized suckling ewes . Furthermore, high circulating levels of prolactin have been associated with low levels of progesterone during early pregnancy, suggesting that hyperprolactinaemia might have a luteolytic effect in the ewe (Rhind, Chesworth & Robinson, 1978) . More recently there have been a number of reports questioning the role of prolactin in both the seasonal and post-partum anoestrus in sheep . McNeilly & Land (1979) concluded that short-term suppression of prolactin secretion did not affect the number of ewes ovulating or corpus luteum progesterone production in LH-RH treated anoestrus ewes . Land et al. (1980) were unable to find an increased proportion of anoestrus ewes discharging LH and FSH in response to oestrogen treatment in ewes that were rendered hyperprolactinaemic by repeated bromocriptine injections . Furthermore, in contrast to-the report of Kann et al. (1977) the suppression of prolactin has proved to be unsuccessful in hastening the onset of reproductive activity in lactating ewes (Louw et al., 1976 ; Ford, 1979 ; Fitzgerald & Cunningham, 1981) . In this study there was no clear relationship between hyperprolactineamia and the duration of post-partum anoestrus . In the local light the onset of activity was earlier in the autumn when prolactin levels were lower than in spring-lambing ewes . In the equatorial light, circulating levels of prolactin were not significantly different between seasons but the performance of PD ewes was markedly lower in the spring . This indicates that levels of prolactin did not play a key role in the persistence of anoestrus in these sheep and that further investigation is required in this field .

ACKNOWLEDGEMENTS The authors thank Mrs K . Cairns and Miss C . Walker for the progesterone radioimmunoassay and Mr S . Haynes for the care of the experimental animals . Financial support for this project was provided by a research grant under scheme R3421, Health and Natural Resources Department, Overseas Development Administration . Reagents for the prolactin radioimmunoassay were kindly supplied by Dr S . Raiti and the NIAMDD . The authors are grateful to Dr A . S . McNeilly for the gift of prolactin antiserum and to Dr A. P . Flint for the progesterone antiserum .

REFERENCES ABRAHAM, G . E ., SWERDLOFF, R ., TULCHINSKY, D . & ODELL, W . D . (1971) . Journal of Clinical Endocrinolog 32, 619 . ALBERT, M . L . (1977) . In Handbook of Radioimmunoassay, ed . G . E . Abraham, p . 179 . New York :

Marcel Decker Inc .



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DUCKER, M . J . & BOWMAN, J . C . (1972) . Animal Production 14, 323 . ERB, R. E ., STTARZ, N . E . & MALVEN, P . V . (1977) . Journal of Dairy Science 60, 197 . FITZGERALD, B . P . & CUNNINGHAM, F . J . (1981) . Journal of Reproduction and Fertility 61, 141 . FLINT, A . F . P ., KINGSTON, E . J., ROBINSON, J . S . & THORBURN, G . D . (1978) . Journal of Endocrinology

78,367 . FORD, J . J . (1979) : Journal of Animal Science 49, 1043. FRASER, C ., GILL, J . C . & ROBINSON, J . J . (1972) . Journal of Physiology 227, 7P. GADSBY, J . E ., HEAP, R . B., HENVILLE, A.& LAING, J . A . (1974) . Journal of Physiology 242, 3P . HAFEZ, E . S . E . (1952) . Journal of Agricultural Science, Cambridge 42, 189 . HUN TER, G . L . (1968a) . Animal Breeding Abstracts 36, 347 . HUNTER, G . L . (1968b) . Animal Breeding Abstracts 36, 533 . HUNTER, G . L . & VAN AARDE, M . R . (1973) . Journal of Reproduction and Fertility 32, 1 . KANN, G . & MARTINET, J . (1975) . Nature, London 257, 63 . KANN, G ., MARTINET, J . & SCHIRAR, A . (1977) . In Prolactin and Human Reproduction, ed . P . G . Crosig-

niani and C . Robin, p . 47 . London : Academic Press . A . (1978) . In Control of Ovulation, ed . D . B . Crighton, G . R. Lamming, p . 319 . London : Butterworths . LAMMING, G . E., MOSELEY, S . R. & MCNEILLY, J . R . (1974) . Journal of Reproduction and Fertility 40 (1), 151 . LAND, R . B ., CARR, W . B ., MCNEILLY, A . S . & PREECE, R . D . (1980) . Journal of Reproduction and Fertility 59, 73 . LOU"', B . P ., LISHMAN, A . W ., BOTHA, W . A ., ARANGIE, P. A . R ., POULTNEY, B . G . & GUNTER, M . J . (1976) . South African Journal of Animal Science 6, 87 . MCNEILLY, A . S. (1980) . Journal of Reproduction and Fertility 58, 537 . MCNEILLY, A . S. & ANDREWS, P . (1974) . Journal of Endocrinology 60, 359 . MCNEILLY, A . S. & LAND, R . B . (1979) . Journal of Reproduction and Fertility 56, 601 . MCNEILLY, J . R ., MOSELEY, S . R . & LAMMING, G . E . (1972) . Journal of Reproduction and Fertility 31, 487 . MAULEON, P . & DAUZIER, L . (1965) . Annales de biologie animale, biochimie et biophysique 5, 131 . MOSELEY, S . R . & LAMMING, G . E . (1969) . Animal Production 11 (2), 284 . PELLETIER, J . (1973). Journal of Reproduction and Fertility 35, 143 . PIJOAN, P. J . (1982) . PhD thesis, University of London, Royal Veterinary College . RHIND, S . M ., CHESWORTH, J . M . & ROBINSON, J . J . (1978) . Journal of Reproduction and Fertility 52, 79 . RHIND, S . M ., ROBINSON, J . J ., CHESWORTH, J . M . & CROFTS, R. M . J . (1980). Journal of Reproduction and Fertility 58, 145 . SEFIDBAKHT, N ., MOSTAFAVI, M . S . & FARID, A . (1977) . Journal of Animal Science 45, 305 . THIMONIER, J ., RAVAULT, J . P . & ORTAVANT, R . (1978) . Annales de biologie animale, biochimie et biophysique 18, 1229 . WILLIAMS, H . LL . (1976) . Journal of Agricultural Science, Cambridge 83, 377 . YEA TES, N . T . M . (1949) . Journal of Agricultural Science, Cambridge 39, 101 . KANN, G ., MARTINET, J . & SCHIRAR, Foxcroft, N . B . Haynes and G . E .

(Accepted forpublication 27April 1984)