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Advancement of ovulation and oestrus after temporary calf removal and FSH supplementation in postpartum beef cows
ANIMAL REPRODUCTION SCIENCE ELSEVIER
Animal Reproduction Science 36 (1994) 1-11
Advancement of ovulation and oestrus after temporary calf removal and FSH supplementation in postpartum beef cows G.M. Rivera*''l,R.H. Alberio", S.S. Callejas b, J.M. Doray a aDepartamento de Producci6n Animal, Estacidn Experimental Agropecuaria Balcarce, Instituto Nacional de Tecnologia Agropecuaria. C.C. 276, (7620) Balcarce, Prov. de Buenos Aires and Laboratorio de Reproduccion y Lactancia (LARLAC-CRICYT), C.C. 855, (5500) Mendoza, , Argentina bFaculty of Veterinary Sciences, Department of Physiology, UNCPBA, (7000) Tandil, Argentina
(Accepted 17 November 1993)
Abstract
To evaluate the effect of temporary calf removal and/or FSH supplementation on postpartum ovarian and oestrous activity, 40 anoestrous multiparous Aberdeen Angus cows under grazing conditions were used. The animals were allocated, on the basis of calving date and body condition, to four initially similar groups according to a 2 X 2 factorial design (ten animals per group) involving a 72 h calf removal (TCR) and exogenous follicle stimulating hormone supplementation (FSH). Anoestrus was determined by measuring plasma progesterone concentrations before treatments, which began at 29.6_ 4.9 days postpartum. Total FSH supplementation ( 12 mg, porcine FSH) was performed by six intramuscular decreasing doses (3, 3, 2, 2, 1 and l rag, respectively) distributed at 12 h intervals, beginning 24 h before TCR. Oestrus detection (twice daily) and blood sample collection (every 2-3 days) were performed from 7 days before the start of treatments and for 45 days thereafter. The TCR plus FSH group had higher oestrous and ovulation rates at 40 days postpartum (control, 10% and 10%; TCR, 10% and 10%; FSH, 10% and 10%; TCR plus FSH, 60% and 60%) and 60 days postpartum (control, 30% and 30%; TCR, 50% and 50%; FSH, 40% and 50%; TCR plus FSH, 80% and 100%). These differences were significant (P< 0.05) for oestrous rates at 40 days postpartum and for ovulation rates at 40 and 60 days postpartum. TCR plus FSH significantly shortened (P< 0.05) the intervals (mean _+ s.e.m., days) from calving to first ovulation (control, 61.2+_5.5; TCR, 62.8 _+4.6; FSH, 61.6 _+3.8 and TCR plus FSH, 43.4_ 3. l ) and a similar trend (P> 0.05) was observed for the intervals from calving to first oestrus (control, 61.2+ 5.5; TCR, *Correspondingauthor. ~Present address: Departamento de Reproducci6n Animal, Facultad de Agronomia y Veterinaria, Univeridad Nacional de Rio Cuarto. Ruta Nac. 36, Km 601. (5800) Rio Cuarto, Argentina. 0378-4320/94/$07.00 © 1994 Eisevier Science Publishers B.V. All rights reserved SSD10378-4320 (93)01292-G
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G.M. Rivera et al./AnimalReproduction Science 36 (1994) 1-11
62.3 + 5.4; FSH, 63.4 + 3.9 and TCR + FSH, 47.7 + 5.2). The rate of short first luteal phases ( ~<10 days) was: control, 40%; TCR, 33%; FSH, 43%; TCR plus FSH, 89% (P<0.12). In summary, TCR plus FSH resulted in increased ovulation and oestrus rates, shorter postpartum intervals, but subnormal corpora lutea were formed following the first ovulation in early postpartum beef cows.
1. Introduction
The productivity of a beef herd depends on its reproductive efficiency. Although a 12 month calving interval is a reasonable biological goal to achieve, some estimations point out that only 50-70% of cows reach this potential ability of producing one calf yearly (INDEC, 1988; Williams, 1990 ). Duration of anoestrus is the main component underlying postpartum infertility and it is affected by two major factors: suckling and nutrition (Short et al., 1990). Another source of postpartum infertility is the short luteal phases following first ovulations, with corpora lutea of shorter-than-normal mean lifespan and of lower capacity to secrete progesterone (Manns et al., 1983; Garverick et al., 1992). This impairs the fertility rate of first oestrus (Short et al., 1972; Odde et al., 1980). The most remarkable endocrine feature of anoestrus in suckled beef cows is chronic suppression of pulsatile luteinizing hormone (LH) release (Rawlings et al., 1980; Humphrey et al., 1983). Although a rise in LH pulse frequency was observed within 24-48 h after temporary weaning (Waiters et al., 1982a; Edwards, 1985; Williams et al., 1987), return of the calf before 96 h markedly attenuated weaning-induced increases in LH secretion and ovulation (Shively and Williams, 1989). Thus, a temporary weaning of 48-72 h may fail to yield a high frequency of ovulation when used alone (Waiters et al., 1982b). The mode of FSH secretion and its role during the postpartum period in cattle are not clear. Several workers have not found pulsatility in FSH secretion and consider that FSH is not a limiting factor for resumption of oestrous cycles (Schams et al., 1978; Lamming et al., 1981; Leung et al., 1986). However, other studies showed pulsatile FSH release (Schallenberger et al., 1982; Williams et al., 1983) and it was concluded that there was an FSH threshold level below which there would be neither follicular development nor sexual reactivation because of the existence of a negative correlation between mean plasma FSH concentrations and the length of anoestrus (Gauthier et al., 1982; Cruz and Kesler, 1988 ). In previous work (R.H. Alberio, unpublished observations, 1986 ) it was stated that exogenous LH plus FSH supplementation was capable of interrupting postpartum anoestrus, but no effect was observed with LH alone. Because temporary calf removal is known to increase LH pulsatility, although the same was not described for FSH (Wright et al., 1987), in the present work we tested the hypothesis that the simultaneous application of a temporary calf removal and exogenous FSH supplementation could improve postpartum sexual activity in beef cows.
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2. Materials and methods
2. I. Animals and experimental design The experiment was conducted in spring and the animals were grazing on a high quality pasture (ryegrass, fescue, wheat grass and white clover); forage availability was not limiting. Forty anoestrous multiparous suckled Aberdeen Angus cows (4-8 years old) were allocated, on the basis of calving date and body condition, to four initially similar groups according to a 2 × 2 factorial design (ten animals per group) involving a 72 h calf removal (TCR) and exogenous follicle stimulating hormone supplementation (FSH). Anoestrus was determined by measuring plasma progesterone concentrations before treatments, which began at 29.6 _+4.9 days postpartum (mean _+s.d. ). Total FSH supplementation ( 12 mg porcine FSH, batch number 90,388 Lab. SANOFI, France) was performed by six intramuscular decreasing doses distributed at 12 h intervals (3, 3, 2, 2, 1 and 1 nag, respectively), beginning 24 h before TCR. This total dose and the duration of the FSH treatment, were the same as used previously (Lishman et al., 1979; R.H. Alberio, unpublished observations, 1986) to induce follicular growth successfully. The calves were removed to a separate paddock out of sound and sight of their dams. Live weight and body condition score of the cows were recorded at 30, 45 and 60 days postpartum. Body condition was determined according to Habich et al. (1974) by dividing body weight by withers height (kg era- 1). Ovarian activity was assessed by plasma progesterone concentrations. Detection of oestrus was carded out by visual observation for 1 h, twice daily during the blood sampling period.
2.2. Blood sampling Blood samples were collected from all cows three times a week (on Mondays, Wednesdays and Fridays) by jugular venipuncture, starting 7 days before the beginning of treatments and for 45 days thereafter. Samples were centrifuged within 1 h of collection and plasma stored at - 2 0 ° C.
2.3. Hormone assay Progesterone concentrations were determined by radioimmunoassay as previously described (Bonavera et al., 1987). Sensitivity of the assay was 0.25 ng m l - 1 and the extraction efficiency was 89%. Intra- and interassay coefficients of variation were 12% (n = 18 ) and 14% (n = 15 ), respectively. Cross reactivity was < 0.02 for other steroids.
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G.M.Riveraet al./AnimalReproduction Science36 (1994) 1-11
2.4. Estimation of the day of ovulation The day of oestrus was considered as the day of ovulation if it was followed by an increase in plasma progesterone concentration above 1 ng m l - ~in at least one sample. Otherwise (ovulations during silent oestrus) ovulation was considered to occur 5 days before two consecutive progesterone elevations of at least 1 ng m1-1 (King, 1984).
2.5. Characterization of the luteal phase The duration of a luteal phase was defined as the period when progesterone concentration was 1 ng m l - ! or more. The first luteal phases were classified according to their length as short or normal. The definition of short luteal cycles as 10 days or less was adopted from Lamming et al. ( 1981 ).
2.6. Statistical analysis Proportions were compared using a X2 test. Ten cows (three, four and three cows from control, TCR and FSH groups, respectively) were still acyclic when blood sampling stopped. Postpartum intervals for these cows were calculated by assuming that ovulation or oestrus occurred on the last day of their blood sampling period. Data of postpartum intervals were analysed by two-way analysis of variance. Duration of the first luteal phases and area under the progesterone curve were compared using the non-parametric Dunn test. Simple correlation analysis was run between the length of first luteal phases and calving-ovulation intervals. References to these statistical procedures are Snedecor and Cochran (1980) and Dunn (1964).
3. Results
3. I. Live weight and body condition Live weights and body condition scores (mean_+s.e.m.) were not different (P> 0.05) among treatments at any time. The mean values of the four groups were: 411_+47 kg and 3.6_+0.33; 428_+53 kg and 3.75_+0.36; 439_+52 kg and 3.86 _+0.37 at 30, 45 and 60 days postpartum, respectively.
3.2. Frequency of oestrus Figure 1 (a) shows the cumulative frequency of heats observed during the postpartum period. The proportion of cows showing oestrus was greater ( P < 0.05 ) in the TCR plus FSH group than in all other groups at 40 days postpartum. There was a similar tendency for subsequent postpartum intervals ( P < 0.2).
G.M. Rivera et al. I Animal Reproduction Science 36 (1994) 1-I1
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Fig. 1. Cumulative oestrous (a) and ovulation (b) rates after temporary calf removal (TCR) and/or FSH supplementation (FSH) in early postpartum beef cows.
3.3. Frequency of ovulations A higher proportion ( P < 0.05 ) of animals in the TCR plus FSH treatment than in all other groups had ovulated at 40, 50 and 60 days postpartum (Fig. 1 (b)). There were no significant differences ( P > 0.05 ) among treatments in the rate of first ovulations with undetected oestrus (silent ovulations: control, 0%; TCR, 17%; FSH, 14% and TCR plus FSH, 30%). All of the animals (n= 10) in the TCR plus FSH group had ovulated by the end of the experiment. From these cows, seven had a second ovulation 13 _+ 1.2 days later (mean_+ s.e.m), and one 32 days later (with a quiescent period after a short first luteal phase). There are no data from the two remaining cows, because the experiment stopped soon after the first ovulation in one of the animals and after a normal first luteal phase in the other cow.
3.4. Postpartum intervals TCR and/or FSH had no effect ( P > 0 . 0 5 ) on the interval (mean _+s.e.m, in days) from calving to first oestrus (control, 61.2_+ 5.5; TCR, 62.3 _+5.4; FSH,
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G.M. Rivera et al./Animal Reproduction Science 36 (1994) 1-11
Table 1 Characteristics of first luteal phases after temporary calf removal (TCR) and/or pFSH supplementation (FSH) in early postpartum beef cows a Group
Control TCR FSH TCR plus FSH
Short phases %
Numbers
40 33 43 89
(2/5) (2/6) (3/7) (8/9)
Length (days, mean + s.e.m. )
Area under the progesterose curve (mean __s.e.m. )
11.02 + 2.4 12.6 + 2.1 10.0+ 1.7 6.60 + 1.2
272 + 95 294 + 70 198+51 118 + 27
"P> 0.05.
63.4 + 3.9 and TCR plus FSH, 47.7 _ 5.2). However, TCR plus FSH shortened significantly (interaction P<0.05) the interval from parturition to first ovulation (control, 61.2 _ 5.5; TCR, 62.8 + 4.6; FSH, 61.6 -+ 3.8 and TCR plus FSH, 43.4_+3.1).
3.5. First luteal phases Features of first luteal phases are shown in Table 1. There were no significant differences (P< 0.05) among treatments either in the length of the first luteal phases or area under the progesterone curve. However, there was a tendency (P<0.12) for a higher rate of short phases in the TCR plus FSH group. A significant (P< 0.05 ) correlation ( r = 0.55 ) was found between duration of the first luteal phase and the interval from calving to first ovulation (y= 1.96 + 0.24x).
4. Discussion
Several factors are known to affect postpartum sexual activity in beef cows (Short et al., 1990 for review). One of them, the suckling stimulus, suppresses pulsatile LH secretion in cows and this endocrine feature seems to play a determinant role in delaying the resumption of postpartum ovarian cycles (Williams, 1990). Thus, several weaning management techniques have been developed to shorten the anoestrous period. Although TCR has been used to improve the postpartum reproductive performance, in the present experiment a 72 h calf removal was unsuccessful in inducing ovulation and oestrus. Studies using TCR (48-72 h) report a decrease (Walters et al., 1982a; Alberio et al., 1984) or no effect (Wright et al., 1987; Bonavera et al., 1990) on postpartum interval length, and this variable response might be partially related to the body condition, the duration of TCR and the stage of follicular development. In this study, the cows had reached the critical target body condition needed to initiate postpartum sexual cycles (Habich et al., 1974) and it seems unlikely that failure of TCR to shorten postpartum interval
G.M. Rivera et al. / Animal Reproduction Science 36 (1994) 1-I1
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was caused by poor body condition as previously reported (Alberio et al., 1984). An alternative explanation for the lack of effect of TCR may be associated with its duration. For example, although an increment in LH pulse frequency was already observed after 24-48 h of TCR (Waiters et al., 1982a; Williams et al., 1987 ), return of the calf before 96 h markedly attenuated weaning-induced increases in LH secretion and ovulation (Shively and Williams, 1989). Regarding follicular development, a greater release of LH with increasing follicular size has been reported in anoestrous cows treated with GnRH (Lishman et al., 1979; Smith et al., 1983 ), and a similar relationship with increasing concentrations of oestrogen was observed in dairy cows (Fernandes et al., 1978). Under our experimental conditions we were not able to measure LH secretion and follicular development. However, the significant interaction between TCR and FSH would suggest that FSH priming may have induced further follicular growth and oestradiol secretion, which in turn, may have acted on the hypothalamo-pituitary axis enhancing its sensitivity to the TCR effects. As previously reviewed (Driancourt, 1991; Roche et ill., 1992), FSH is mainly responsible for recruitment and selection of the dominant follicle, and exposure of an oestrogen-producing dominant follicle to frequent LH pulses is the key to final maturation and ovulation of this follicle. In two previous studies (Lishman et al., 1979; Sheffel et al., 1982) exogenous FSH treatment increased follicular growth, but the ovulation rate was not changed. It is well known that calf removal increases LH pulsatility, but the same was not observed for FSH (Carruthers et al., 1980; Convey et al., 1983; Wright et al., 1987). Therefore, during the postpartum period as in the oestrous cycle, it seems probable that both factors, an appropriate FSH-induced follicular growth and a high frequency of pulsatile LH release, are necessary to induce ovulation and oestrus. It has been observed that declining levels of FSH with increasing concentrations of LH during the follicular phase may be sufficient to develop the dominant ovulatory follicle (Kaneko et al., 1991 ). We suggest that this physiological situation may have been recreated in our FSH-primed weaned anoestrous cows. The present experiment shows that a combination of 72 h calf removal plus FSH treatment significantly advances the initiation of sexual cycles in postpartum beef cows. These findings agree with an earlier study (R.H. Alberio, unpublished observations, 1986) in which exogenous LH (intravenous pulses at 2 h intervals) or LH plus FSH were given to suckled beef cows at 22-50 days postpartum. LH plus FSH resulted in follicular growth in 75% and ovulation in 56% of treated cows (n = 16 ), whereas with LH alone only one of 13 cows had ovulated within 6 days after treatments. Collectively, these observations lead us to reconsider the relative contributions of LH and FSH in inducing sexual cycles during the postpartum period. In seasonally anoestrous ewes, continued pulsatile treatment with GnRH (McLeod et al., 1982a,b), but not LH (McNatty et al., 1984) resulted in continued follicle growth, ovulation and luteal function. Treatment with GnRH maintained the plasma concentrations of FSH, while LH treatment was associated with a reduction in FSH. Furthermore, suppression of FSH by injection of bovine follicular fluid during the treatment of anoestrous ewes
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G.M. Rivera et al./Animal Reproduction Science 36 (1994) 1-11
with pulsatile GnRH prevented ovulation (McLeod and McNeilly, 1987), confirming the requirements for FSH for normal follicle growth during anoestrus. Similarly, in postpartum beef cows, successful ovulation has been related to increases in FSH secretion (Gauthier et al., 1982; Cruz and Kesler, 1988 ) and on the contrary, administration of steroid-free follicular fluid suppressed concentrations of FSH and delayed ovulation (Hinshelwood et al., 1987 ). In CmRH agonist treated ewes (Picton et al., 1990) the infusion of ovine FSH alone in the presence of basal concentrations but non-pulsatile secretion of LH resulted in a time-dependent increase in preovulatory follicle growth and an increase in the number of oestrogenic follicles. The higher FSH availability in FSHtreated cows could have increased follicle viability throughout an increased aromatase activity (McNatty et al., 1985 ). This could be related to secretion of autocrine and paracrine factors which amplify FSH action. IGF-I (Adashi et al., 1985) and TGF-fl (Lobb and Dorrington, 1992), seem to stimulate FSH-induced aromatase activity, which in turn increases oestradiol levels, as well as LH receptors. Hence, it is possible that FSH-primed follicles were in a responsive state to ovulate effectively in response to the TCR-induced LH pulse secretion. Regarding the quality of the first luteal phases, there was a trend for a higher rate of short phases, with a lower area under the progesterone curve in the TCR plus FSH cows. When sexual cycles were induced with a combined treatment of oestradiol benzoate plus TCR in early postpartum cows, a similar rate (87.5%) of short-lived corpora lutea was observed (Callejas et al., 1992). On the other hand, we found a positive relationship between length of postpartum interval and the duration of the first luteal phase, which agrees with previous reports (Eger et al., 1988). It seems probable that these short-lived corpora lutea may be caused by a premature release of P G F 2 a from the uterus, rather than a suboptimal priming of the preovulatory follicle with gonadotrophins or reduced luteotrophic support of the corpus luteum (Baird, 1992). Although TCR plus FSH treatment resulted in a higher incidence of initial short luteal phases, the earlier resumption of ovarian activity might result in higher fertility rates of subsequent oestrous cycles. Seven often cows from the TCR plus FSH group had a second ovulation 13 +_1.2 days later followed by a normal luteal phase (data not shown). It has been shown that inseminations carried out in an oestrous period which had been preceded by progesterone increases were more fertile than those where no prior progesterone peak existed (Corah et al., 1974). In summary, TCR plus FSH resulted in increased ovulation and oestrous rates, shorter postpartum intervals, but subnormal corpora lutea were formed following first ovulations in early postpartum beef cows.
Acknowledgements We thank Carlos Lobato, Natividad Ferreira and the staff of the Experimental Field number 6 of the Experimental Station at Balcarce for their excellent assis-
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tance. We also thank Drs. Alfredo Castro-Vazquez and Graciela A. Jahn of LARLAC-CRICYT for helpful criticism of the manuscript. References Adashi, E.Y., Resnick, C.E., Brodie, A.M., Svoboda, M.E. and Van Wyk, J.J., 1985. Somatomedin C mediated potentiation of follicle stimulating hormone induced aromatase activity of cultured rat granulosa cells. Endocrinology, 117:2313-2320. Alberio, R., Butler, H.M., Palma, G., Schiersmann, G.C.S., Algorta, D. and Ortiz, A., 1984. Actividad reproductiva y fertilidad luego de un destete temporario en vacas de cria multiparas con diferentes estados corporales. Rev. Arg. Prod. Anim., 4: 555-566. Baird, D.T., 1992. Luteotrophic control of the corpus luteum. Anim. Reprod. Sci., 28: 95-102. Bonavera, J.J., Verg6s, E. and Tortonese, D.J., 1987. Radioimmunoanalisisde progesterona en plasma bovino. Comparaci6n del uso del 125I y del 3H como trazadores. Acta Bioq. Clin. Latinoamericana, 21: 67-74. Bonavera, J.J., Schiersmann, G.C.S., Alberio, R.H. and Mestre, J., 1990. A note on the effects of 72hour calf removal and/or bull exposure upon post-partum reproductive performance. Anim. Prod., 50: 202-206. CaUejas, S.S., Alberio, R., Doray, J., Schiersmann, G. and Teruel, M., 1992. Caracteristicas de los ciclos estrales inducidos por el destete temporario, benzoato de estradiol y la combinaci6n de ambos en el postparto de vacas de cria. XIII Congreso Panamericano de Ciencias Veterinarias. Santiago, Chile. Abstract, p. 27. Carruthers, T.D., Convey, E.M., Kesner, J.S., Hafs, H.D. and Cheng, K.W., 1980. The hypothalamopituitary gonadotrophic axis of suckled and nonsuckled dairy cows postpartum. J. Anim. Sci., 51: 949-957. Convey, E.M., Tucker, H.A. and Short, R.E., 1983. Acute effect of suckling on gonadotropin, prolactin and glucocorticoid concentrations in serum of intact and ovarieetomised beef cows. Theriogenology, 20:661-674. Corah, L.R., Weel, A.P., Dunn, T.G. and Kaltenbach, C.C., 1974. Prepartum and postpartum levels of progesterone and estradiol in beef heifers fed two levels of energy. J. Anim. Sci., 39: 380-385. Cruz, C.L. and Kesler, D.J., 1988. Relationships of GnRH induced LH and FSH profiles on the ovulation responses and corpus luteum function of postpartum suckled cows. In: 1lth International Congress on Animal Reproduction and A.I. Dublin, Ireland. Vol l, p. 18. Driancourt, M.A., 199 I. Follicular dynamics in sheep and cattle. Theriogenology, 35: 55-79. Dunn, O.J., 1964. Multiple comparisons using rank sums. Technometrics, 6:241-252. Edwards, S., 1985. The effects of short term calf removal on pulsatile secretion in the postpartum beef cows. Theriogenology, 23: 777-785. Eger, S., Shemesh, M., Schindler, H., Amir, S. and Foote, R.H., 1988. Characterization of short luteal cycles in the early post-partum period and their relation to reproductive performance of dairy cows. Anim. Reprod. Sci., 16:215-224. Fernandes, L.C., Thatcher, W.W., Wilcox, C.J. and Call, E.P., 1978. LH release in response to GnRH during the postpartum period of dairy cows. J. Anim. Sci., 46: 443-448. Garverick, H.A., Zollers, W.G. and Smith, M.F., 1992. Mechanisms associated with corpus luteum lifespan in animals having normal or subnormal luteal function. Anim. Reprod. Sci., 28:11 l - 124. Gauthier, D., Blanc, M.R., Petit, M. and Pelletier, J., 1982. FSH and LH variation in beef cows during the postpartum period. Reprod. Nutr. Dev., 22: 283-290. Habich, G.E., Verde, L., Schiersmann, G.C.S. and Carrillo, J., 1974. Efecto de la restricci6n en el aporte energ6tico seguida de realimentaci6n sobre la reanudaci6n de los ciclos estrales de vacas Aberdeen Angus post-partum. Prod. Anim., 5:11 l-128. Hinshelwood, M.M., Dierschke, D.J. and Hauser, E.R., 1987. The effect of bovine follicular fluid on follicle-stimulating hormone (FSH) concentrations in beef cows in the early postpartum period. Biol. Reprod., 36: Suppl. 1,153. Humphrey, W.D., Kaltenbach, C.C., Dunn, T.G., Koritnik, D.R. and Niswender, G.D., 1983. Char-
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acterization of hormonal patterns in beef cows during the postpartum anestrus. J. Anim. Sci., 56: 445-453. INDEC, 1988. Censo Nacional Agropecuario. Ministerio de Economia. Buenos Aires, Argentina. Kaneko, H., Terada, T., Taya, K., Watanabe, G., Sasamoto, S. Hasegawa, Y. and Igarashi, M., 1991. Ovarian follicular dynamics and concentrations of oestradiol-17p, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow. Reprod. Fertil. Dev., 3: 529-535. King, G.J., 1984. Normal, short and long postpartum estrous cycles in dairy and beef cows. In: Proc. X Int. Cong. Animal Reproduction and A.I. Illinois, Vol. 3, pp. 399-401. Lamming, G.E., Wathes, D.C. and Peters, A.R., 1981. Endocrine patterns of the postpartum cows. J. Reprod. Fertil. Suppl. 30: 155-170. Leung, K., Padmanabhan, V., Spicer, L.J., Tucker, H.A., Short, R.E. and Convey, E.M., 1986. Relationship between pituitary GnRH-binding sites and pituitary release of gonadotrophins in postpartum beef cows. J. Reprod. Fertil., 76: 53-63. Lishman, A.W., Allison, R.L., Fogwell, R.L., Butcher, R.L. and Inskeep, E.K., 1979. Follicular development and function of induced corpora lutea in underfed postpartum anestrous beef cows. J. Anita. Sci., 48: 867-875. Lobb, D.K. and Dorrington, J., 1992. Intraovarian regulation of follicular development. Anita. Reprod. Sci., 28: 343-354. Manns, J.G., Humphrey, W.D., Flood, R.J., Mapletoft, R.J., Rawlings, N. and Cheng, K.W., 1983. Endocrine profiles and functional characteristics of corpora lutea following onset of postpartum ovarian activity in beef cows. Can. J. Anita. Sci., 63:331-347. McLeod, B.J. and McNeilly, A.S., 1987. Suppression of plasma FSH concentrations with bovine follicular fluid blocks ovulation in GnRH-treated seasonally anoestrous ewes. J. Reprod. Fertil., 81: 187-194. McLeod, B.J., Haresign, W. and Lamming, G.E., 1982a. The induction of ovulation and luteal function in seasonally anoestrous ewes treated with small-dose multiple injections of GnRH. J. Reprod. Fertil., 65:215-221. McLeod, B.J., Haresign, W. and Lamming, G.E., 1982b. Response of seasonally anoestrous ewes to small-dose multiple injections of GnRH with and without progesterone treatment. J. Reprod. Fertil., 65: 223-230. McNatty, K.P., Hudson, N., Gibb, M., Ball, K., Fannin, J., Kieboom, L. and Thurley, D.C., 1984. Effects of long-term treatment with LH on induction of cyclic ovarian activity in seasonally anoestrous ewes. J. Endocrinol., 100: 67-73. McNatty, K.P., Hudson, N., Gibb, M., Ball, K., Henderson, K.M., Heath, D.A., Lun, S. and Kieboom, L.E., 1985. FSH influences follicle viability, oestradiol biosynthesis and ovulation rate in Romney ewes. J. Reprod. Fertil., 75: 121-131. Odde, K.G., Ward, H.S., Kiracofe, G.H., Mc Kee, R.M. and Kittok, R.J., 1980. Short estrous cycles and associated serum progesterone levels in beef cows. Theriogenology, 14:105-112. Picton, H.M., Tsonis, C.G. and McNeilly, A.S., 1990. FSH causes a time-dependent stimulation of preovulatory follicle growth in the absence of pulsatile LH secretion in ewes chronically treated with gonadotrophin-releasing hormone. J. Endocrinol., 126: 297-307. Rawlings, N.C., Weir, L., Todd, B., Manns, J. and Hyland, J.H., 1980. Some endocrine changes associated with the postpartum period of the suckling beef cow. J. Reprod. Fertil., 60:301-308. Roche, J.F., Crowc, M.A. and Boland, M.P., 1992. Postpartum anoestrus in dairy and beef cows. Anita. Reprod. Sci., 28: 371-378. Schallenberger, E., Oerterer, U. and Hutterer, G., 1982. Neuroendocrine regulation of post-partum function. In: H. Karg and E. Schallenberger (Editors), Factors Influencing Fertility in the Postpartum Cow. Current Topics of Veterinary Medicine and Animal Science. Martinus Nijhoff, The Hague, Vol 20, pp. 123-147. Schams, D., Schallemberger, E., Menzer, Ch., Stangl, J., Zottmeir, K., Hoffman, B. and Karg, H., 1978. Profiles of LH, FSH and progesterone in post-partum dairy cows and their relation to the commencement of cyclic functions. Theriogenology, 10: 453-468. Sheffel, C.E., Pratt, B.R., Ferrel, W.L. and Inskeep, E.K., 1982. Induced corpora lutea in the postpar-
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tum beef cow. II. Effects of treatment with progestogen and gonadotropins. J. Anim. Sci., 54: 830835. Shively, T.E. and Williams, G.L., 1989. Patterns of tonic luteinizing hormone release and ovulation frequency in suckled anestrous beef cows following varying intervals of temporary weaning. Domest. Anim. Endocrinol., 6: 379-387. Short, R.E., Bellows, R.H., Moody, E.L. and Howland, B.E., 1972. Effect of suckling and mastectomy on bovine postpartum reproduction. J. Anim. Sci., 34: 70-74. Short, R.E., Bellows, R.H., Staigmiller, R.B., Berardinelli, J.G. and Custer, E.E., 1990. Physiological mechanisms controlling anestrus and infertility in postpartum beef cattle. J. Anim. Sci., 68: 799816. Smith, M.F., Lishman, A.W., Lewis, G.S., Harms, P.G., Ellersieck, M.R., Inskeep, E.K., Wiltbank, J.N. and Amoss, M.S., 1983. Pituitary and ovarian responses to gonadotropin releasing hormone, calf removal and progestogen in anestrous beef cows. J. Anim. Sci., 57: 418-424. Snedecor, G.W. and Cochran, W.G., 1980. Statistical Methods. Iowa State University Press, Ames, IA. Waiters, D.L., Kaltenbach, C.C., Dunn, T.G. and Short, R.E., 1982a. Pituitary and ovarian function in postpartum beef cows. I. Effect of suckling on serum and follicular fluid hormones and follicular gonadotropin receptors. Biol. Reprod., 26: 640-646. Walters, D.L., Smith, M.F., Harms, P.G. and Wiltbank, J.N., 1982b. Effects of steroids and/or 48 hr calf removal on serum luteinizing hormone concentrations in anestrous beef cows. Theriogenology, 18: 349-355. Williams, G.L., 1990. Suckling as regulator of postpartum rebreeding in cattle: a review. J. Anim. Sci., 68: 831-852. Williams, G.L., Talavera, F., Petersen, J.B., Kirsch, J.D. and Tilton, J.E., 1983. Coincident secretion of follicle-stimulating hormone and luteinizinghormone in postpartum beef cows: effects of suckling and low level increases of systemic progesterone. Biol. Reprod., 29: 362-373. Williams, G.L., Koziorowski, M., Osborn, R.G., Kirsch, J.D. and Slanger, W.D., 1987. The postweaning rise of tonic luteinizinghormone secretion in anestrous cows is not prevented by chronic milking or the physical presence of the calf. Biol. Reprod., 36:1079-1084. Wright, I.A., Rhind, S.M., Russel, J.F., Whyte, T.K., McBean, A.J. and McMillen, S.R., 1987. Effects of body condition, food intake and temporary calf separation on the duration of the post-partum anoestrous period and associated LH, FSH and prolactin concentrations in beef cows. Anim. Prod., 45: 395-402.
Animal Reproduction Science 36 (1994) 1-11
Advancement of ovulation and oestrus after temporary calf removal and FSH supplementation in postpartum beef cows G.M. Rivera*''l,R.H. Alberio", S.S. Callejas b, J.M. Doray a aDepartamento de Producci6n Animal, Estacidn Experimental Agropecuaria Balcarce, Instituto Nacional de Tecnologia Agropecuaria. C.C. 276, (7620) Balcarce, Prov. de Buenos Aires and Laboratorio de Reproduccion y Lactancia (LARLAC-CRICYT), C.C. 855, (5500) Mendoza, , Argentina bFaculty of Veterinary Sciences, Department of Physiology, UNCPBA, (7000) Tandil, Argentina
(Accepted 17 November 1993)
Abstract
To evaluate the effect of temporary calf removal and/or FSH supplementation on postpartum ovarian and oestrous activity, 40 anoestrous multiparous Aberdeen Angus cows under grazing conditions were used. The animals were allocated, on the basis of calving date and body condition, to four initially similar groups according to a 2 X 2 factorial design (ten animals per group) involving a 72 h calf removal (TCR) and exogenous follicle stimulating hormone supplementation (FSH). Anoestrus was determined by measuring plasma progesterone concentrations before treatments, which began at 29.6_ 4.9 days postpartum. Total FSH supplementation ( 12 mg, porcine FSH) was performed by six intramuscular decreasing doses (3, 3, 2, 2, 1 and l rag, respectively) distributed at 12 h intervals, beginning 24 h before TCR. Oestrus detection (twice daily) and blood sample collection (every 2-3 days) were performed from 7 days before the start of treatments and for 45 days thereafter. The TCR plus FSH group had higher oestrous and ovulation rates at 40 days postpartum (control, 10% and 10%; TCR, 10% and 10%; FSH, 10% and 10%; TCR plus FSH, 60% and 60%) and 60 days postpartum (control, 30% and 30%; TCR, 50% and 50%; FSH, 40% and 50%; TCR plus FSH, 80% and 100%). These differences were significant (P< 0.05) for oestrous rates at 40 days postpartum and for ovulation rates at 40 and 60 days postpartum. TCR plus FSH significantly shortened (P< 0.05) the intervals (mean _+ s.e.m., days) from calving to first ovulation (control, 61.2+_5.5; TCR, 62.8 _+4.6; FSH, 61.6 _+3.8 and TCR plus FSH, 43.4_ 3. l ) and a similar trend (P> 0.05) was observed for the intervals from calving to first oestrus (control, 61.2+ 5.5; TCR, *Correspondingauthor. ~Present address: Departamento de Reproducci6n Animal, Facultad de Agronomia y Veterinaria, Univeridad Nacional de Rio Cuarto. Ruta Nac. 36, Km 601. (5800) Rio Cuarto, Argentina. 0378-4320/94/$07.00 © 1994 Eisevier Science Publishers B.V. All rights reserved SSD10378-4320 (93)01292-G
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G.M. Rivera et al./AnimalReproduction Science 36 (1994) 1-11
62.3 + 5.4; FSH, 63.4 + 3.9 and TCR + FSH, 47.7 + 5.2). The rate of short first luteal phases ( ~<10 days) was: control, 40%; TCR, 33%; FSH, 43%; TCR plus FSH, 89% (P<0.12). In summary, TCR plus FSH resulted in increased ovulation and oestrus rates, shorter postpartum intervals, but subnormal corpora lutea were formed following the first ovulation in early postpartum beef cows.
1. Introduction
The productivity of a beef herd depends on its reproductive efficiency. Although a 12 month calving interval is a reasonable biological goal to achieve, some estimations point out that only 50-70% of cows reach this potential ability of producing one calf yearly (INDEC, 1988; Williams, 1990 ). Duration of anoestrus is the main component underlying postpartum infertility and it is affected by two major factors: suckling and nutrition (Short et al., 1990). Another source of postpartum infertility is the short luteal phases following first ovulations, with corpora lutea of shorter-than-normal mean lifespan and of lower capacity to secrete progesterone (Manns et al., 1983; Garverick et al., 1992). This impairs the fertility rate of first oestrus (Short et al., 1972; Odde et al., 1980). The most remarkable endocrine feature of anoestrus in suckled beef cows is chronic suppression of pulsatile luteinizing hormone (LH) release (Rawlings et al., 1980; Humphrey et al., 1983). Although a rise in LH pulse frequency was observed within 24-48 h after temporary weaning (Waiters et al., 1982a; Edwards, 1985; Williams et al., 1987), return of the calf before 96 h markedly attenuated weaning-induced increases in LH secretion and ovulation (Shively and Williams, 1989). Thus, a temporary weaning of 48-72 h may fail to yield a high frequency of ovulation when used alone (Waiters et al., 1982b). The mode of FSH secretion and its role during the postpartum period in cattle are not clear. Several workers have not found pulsatility in FSH secretion and consider that FSH is not a limiting factor for resumption of oestrous cycles (Schams et al., 1978; Lamming et al., 1981; Leung et al., 1986). However, other studies showed pulsatile FSH release (Schallenberger et al., 1982; Williams et al., 1983) and it was concluded that there was an FSH threshold level below which there would be neither follicular development nor sexual reactivation because of the existence of a negative correlation between mean plasma FSH concentrations and the length of anoestrus (Gauthier et al., 1982; Cruz and Kesler, 1988 ). In previous work (R.H. Alberio, unpublished observations, 1986 ) it was stated that exogenous LH plus FSH supplementation was capable of interrupting postpartum anoestrus, but no effect was observed with LH alone. Because temporary calf removal is known to increase LH pulsatility, although the same was not described for FSH (Wright et al., 1987), in the present work we tested the hypothesis that the simultaneous application of a temporary calf removal and exogenous FSH supplementation could improve postpartum sexual activity in beef cows.
G.M. Rivera et al. / Animal Reproduction Science 36 (1994) 1-11
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2. Materials and methods
2. I. Animals and experimental design The experiment was conducted in spring and the animals were grazing on a high quality pasture (ryegrass, fescue, wheat grass and white clover); forage availability was not limiting. Forty anoestrous multiparous suckled Aberdeen Angus cows (4-8 years old) were allocated, on the basis of calving date and body condition, to four initially similar groups according to a 2 × 2 factorial design (ten animals per group) involving a 72 h calf removal (TCR) and exogenous follicle stimulating hormone supplementation (FSH). Anoestrus was determined by measuring plasma progesterone concentrations before treatments, which began at 29.6 _+4.9 days postpartum (mean _+s.d. ). Total FSH supplementation ( 12 mg porcine FSH, batch number 90,388 Lab. SANOFI, France) was performed by six intramuscular decreasing doses distributed at 12 h intervals (3, 3, 2, 2, 1 and 1 nag, respectively), beginning 24 h before TCR. This total dose and the duration of the FSH treatment, were the same as used previously (Lishman et al., 1979; R.H. Alberio, unpublished observations, 1986) to induce follicular growth successfully. The calves were removed to a separate paddock out of sound and sight of their dams. Live weight and body condition score of the cows were recorded at 30, 45 and 60 days postpartum. Body condition was determined according to Habich et al. (1974) by dividing body weight by withers height (kg era- 1). Ovarian activity was assessed by plasma progesterone concentrations. Detection of oestrus was carded out by visual observation for 1 h, twice daily during the blood sampling period.
2.2. Blood sampling Blood samples were collected from all cows three times a week (on Mondays, Wednesdays and Fridays) by jugular venipuncture, starting 7 days before the beginning of treatments and for 45 days thereafter. Samples were centrifuged within 1 h of collection and plasma stored at - 2 0 ° C.
2.3. Hormone assay Progesterone concentrations were determined by radioimmunoassay as previously described (Bonavera et al., 1987). Sensitivity of the assay was 0.25 ng m l - 1 and the extraction efficiency was 89%. Intra- and interassay coefficients of variation were 12% (n = 18 ) and 14% (n = 15 ), respectively. Cross reactivity was < 0.02 for other steroids.
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G.M.Riveraet al./AnimalReproduction Science36 (1994) 1-11
2.4. Estimation of the day of ovulation The day of oestrus was considered as the day of ovulation if it was followed by an increase in plasma progesterone concentration above 1 ng m l - ~in at least one sample. Otherwise (ovulations during silent oestrus) ovulation was considered to occur 5 days before two consecutive progesterone elevations of at least 1 ng m1-1 (King, 1984).
2.5. Characterization of the luteal phase The duration of a luteal phase was defined as the period when progesterone concentration was 1 ng m l - ! or more. The first luteal phases were classified according to their length as short or normal. The definition of short luteal cycles as 10 days or less was adopted from Lamming et al. ( 1981 ).
2.6. Statistical analysis Proportions were compared using a X2 test. Ten cows (three, four and three cows from control, TCR and FSH groups, respectively) were still acyclic when blood sampling stopped. Postpartum intervals for these cows were calculated by assuming that ovulation or oestrus occurred on the last day of their blood sampling period. Data of postpartum intervals were analysed by two-way analysis of variance. Duration of the first luteal phases and area under the progesterone curve were compared using the non-parametric Dunn test. Simple correlation analysis was run between the length of first luteal phases and calving-ovulation intervals. References to these statistical procedures are Snedecor and Cochran (1980) and Dunn (1964).
3. Results
3. I. Live weight and body condition Live weights and body condition scores (mean_+s.e.m.) were not different (P> 0.05) among treatments at any time. The mean values of the four groups were: 411_+47 kg and 3.6_+0.33; 428_+53 kg and 3.75_+0.36; 439_+52 kg and 3.86 _+0.37 at 30, 45 and 60 days postpartum, respectively.
3.2. Frequency of oestrus Figure 1 (a) shows the cumulative frequency of heats observed during the postpartum period. The proportion of cows showing oestrus was greater ( P < 0.05 ) in the TCR plus FSH group than in all other groups at 40 days postpartum. There was a similar tendency for subsequent postpartum intervals ( P < 0.2).
G.M. Rivera et al. I Animal Reproduction Science 36 (1994) 1-I1
100
O ...... O Control A--A TCR O--O FSH t - - ~ TCR+FSH
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Fig. 1. Cumulative oestrous (a) and ovulation (b) rates after temporary calf removal (TCR) and/or FSH supplementation (FSH) in early postpartum beef cows.
3.3. Frequency of ovulations A higher proportion ( P < 0.05 ) of animals in the TCR plus FSH treatment than in all other groups had ovulated at 40, 50 and 60 days postpartum (Fig. 1 (b)). There were no significant differences ( P > 0.05 ) among treatments in the rate of first ovulations with undetected oestrus (silent ovulations: control, 0%; TCR, 17%; FSH, 14% and TCR plus FSH, 30%). All of the animals (n= 10) in the TCR plus FSH group had ovulated by the end of the experiment. From these cows, seven had a second ovulation 13 _+ 1.2 days later (mean_+ s.e.m), and one 32 days later (with a quiescent period after a short first luteal phase). There are no data from the two remaining cows, because the experiment stopped soon after the first ovulation in one of the animals and after a normal first luteal phase in the other cow.
3.4. Postpartum intervals TCR and/or FSH had no effect ( P > 0 . 0 5 ) on the interval (mean _+s.e.m, in days) from calving to first oestrus (control, 61.2_+ 5.5; TCR, 62.3 _+5.4; FSH,
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G.M. Rivera et al./Animal Reproduction Science 36 (1994) 1-11
Table 1 Characteristics of first luteal phases after temporary calf removal (TCR) and/or pFSH supplementation (FSH) in early postpartum beef cows a Group
Control TCR FSH TCR plus FSH
Short phases %
Numbers
40 33 43 89
(2/5) (2/6) (3/7) (8/9)
Length (days, mean + s.e.m. )
Area under the progesterose curve (mean __s.e.m. )
11.02 + 2.4 12.6 + 2.1 10.0+ 1.7 6.60 + 1.2
272 + 95 294 + 70 198+51 118 + 27
"P> 0.05.
63.4 + 3.9 and TCR plus FSH, 47.7 _ 5.2). However, TCR plus FSH shortened significantly (interaction P<0.05) the interval from parturition to first ovulation (control, 61.2 _ 5.5; TCR, 62.8 + 4.6; FSH, 61.6 -+ 3.8 and TCR plus FSH, 43.4_+3.1).
3.5. First luteal phases Features of first luteal phases are shown in Table 1. There were no significant differences (P< 0.05) among treatments either in the length of the first luteal phases or area under the progesterone curve. However, there was a tendency (P<0.12) for a higher rate of short phases in the TCR plus FSH group. A significant (P< 0.05 ) correlation ( r = 0.55 ) was found between duration of the first luteal phase and the interval from calving to first ovulation (y= 1.96 + 0.24x).
4. Discussion
Several factors are known to affect postpartum sexual activity in beef cows (Short et al., 1990 for review). One of them, the suckling stimulus, suppresses pulsatile LH secretion in cows and this endocrine feature seems to play a determinant role in delaying the resumption of postpartum ovarian cycles (Williams, 1990). Thus, several weaning management techniques have been developed to shorten the anoestrous period. Although TCR has been used to improve the postpartum reproductive performance, in the present experiment a 72 h calf removal was unsuccessful in inducing ovulation and oestrus. Studies using TCR (48-72 h) report a decrease (Walters et al., 1982a; Alberio et al., 1984) or no effect (Wright et al., 1987; Bonavera et al., 1990) on postpartum interval length, and this variable response might be partially related to the body condition, the duration of TCR and the stage of follicular development. In this study, the cows had reached the critical target body condition needed to initiate postpartum sexual cycles (Habich et al., 1974) and it seems unlikely that failure of TCR to shorten postpartum interval
G.M. Rivera et al. / Animal Reproduction Science 36 (1994) 1-I1
7
was caused by poor body condition as previously reported (Alberio et al., 1984). An alternative explanation for the lack of effect of TCR may be associated with its duration. For example, although an increment in LH pulse frequency was already observed after 24-48 h of TCR (Waiters et al., 1982a; Williams et al., 1987 ), return of the calf before 96 h markedly attenuated weaning-induced increases in LH secretion and ovulation (Shively and Williams, 1989). Regarding follicular development, a greater release of LH with increasing follicular size has been reported in anoestrous cows treated with GnRH (Lishman et al., 1979; Smith et al., 1983 ), and a similar relationship with increasing concentrations of oestrogen was observed in dairy cows (Fernandes et al., 1978). Under our experimental conditions we were not able to measure LH secretion and follicular development. However, the significant interaction between TCR and FSH would suggest that FSH priming may have induced further follicular growth and oestradiol secretion, which in turn, may have acted on the hypothalamo-pituitary axis enhancing its sensitivity to the TCR effects. As previously reviewed (Driancourt, 1991; Roche et ill., 1992), FSH is mainly responsible for recruitment and selection of the dominant follicle, and exposure of an oestrogen-producing dominant follicle to frequent LH pulses is the key to final maturation and ovulation of this follicle. In two previous studies (Lishman et al., 1979; Sheffel et al., 1982) exogenous FSH treatment increased follicular growth, but the ovulation rate was not changed. It is well known that calf removal increases LH pulsatility, but the same was not observed for FSH (Carruthers et al., 1980; Convey et al., 1983; Wright et al., 1987). Therefore, during the postpartum period as in the oestrous cycle, it seems probable that both factors, an appropriate FSH-induced follicular growth and a high frequency of pulsatile LH release, are necessary to induce ovulation and oestrus. It has been observed that declining levels of FSH with increasing concentrations of LH during the follicular phase may be sufficient to develop the dominant ovulatory follicle (Kaneko et al., 1991 ). We suggest that this physiological situation may have been recreated in our FSH-primed weaned anoestrous cows. The present experiment shows that a combination of 72 h calf removal plus FSH treatment significantly advances the initiation of sexual cycles in postpartum beef cows. These findings agree with an earlier study (R.H. Alberio, unpublished observations, 1986) in which exogenous LH (intravenous pulses at 2 h intervals) or LH plus FSH were given to suckled beef cows at 22-50 days postpartum. LH plus FSH resulted in follicular growth in 75% and ovulation in 56% of treated cows (n = 16 ), whereas with LH alone only one of 13 cows had ovulated within 6 days after treatments. Collectively, these observations lead us to reconsider the relative contributions of LH and FSH in inducing sexual cycles during the postpartum period. In seasonally anoestrous ewes, continued pulsatile treatment with GnRH (McLeod et al., 1982a,b), but not LH (McNatty et al., 1984) resulted in continued follicle growth, ovulation and luteal function. Treatment with GnRH maintained the plasma concentrations of FSH, while LH treatment was associated with a reduction in FSH. Furthermore, suppression of FSH by injection of bovine follicular fluid during the treatment of anoestrous ewes
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G.M. Rivera et al./Animal Reproduction Science 36 (1994) 1-11
with pulsatile GnRH prevented ovulation (McLeod and McNeilly, 1987), confirming the requirements for FSH for normal follicle growth during anoestrus. Similarly, in postpartum beef cows, successful ovulation has been related to increases in FSH secretion (Gauthier et al., 1982; Cruz and Kesler, 1988 ) and on the contrary, administration of steroid-free follicular fluid suppressed concentrations of FSH and delayed ovulation (Hinshelwood et al., 1987 ). In CmRH agonist treated ewes (Picton et al., 1990) the infusion of ovine FSH alone in the presence of basal concentrations but non-pulsatile secretion of LH resulted in a time-dependent increase in preovulatory follicle growth and an increase in the number of oestrogenic follicles. The higher FSH availability in FSHtreated cows could have increased follicle viability throughout an increased aromatase activity (McNatty et al., 1985 ). This could be related to secretion of autocrine and paracrine factors which amplify FSH action. IGF-I (Adashi et al., 1985) and TGF-fl (Lobb and Dorrington, 1992), seem to stimulate FSH-induced aromatase activity, which in turn increases oestradiol levels, as well as LH receptors. Hence, it is possible that FSH-primed follicles were in a responsive state to ovulate effectively in response to the TCR-induced LH pulse secretion. Regarding the quality of the first luteal phases, there was a trend for a higher rate of short phases, with a lower area under the progesterone curve in the TCR plus FSH cows. When sexual cycles were induced with a combined treatment of oestradiol benzoate plus TCR in early postpartum cows, a similar rate (87.5%) of short-lived corpora lutea was observed (Callejas et al., 1992). On the other hand, we found a positive relationship between length of postpartum interval and the duration of the first luteal phase, which agrees with previous reports (Eger et al., 1988). It seems probable that these short-lived corpora lutea may be caused by a premature release of P G F 2 a from the uterus, rather than a suboptimal priming of the preovulatory follicle with gonadotrophins or reduced luteotrophic support of the corpus luteum (Baird, 1992). Although TCR plus FSH treatment resulted in a higher incidence of initial short luteal phases, the earlier resumption of ovarian activity might result in higher fertility rates of subsequent oestrous cycles. Seven often cows from the TCR plus FSH group had a second ovulation 13 +_1.2 days later followed by a normal luteal phase (data not shown). It has been shown that inseminations carried out in an oestrous period which had been preceded by progesterone increases were more fertile than those where no prior progesterone peak existed (Corah et al., 1974). In summary, TCR plus FSH resulted in increased ovulation and oestrous rates, shorter postpartum intervals, but subnormal corpora lutea were formed following first ovulations in early postpartum beef cows.
Acknowledgements We thank Carlos Lobato, Natividad Ferreira and the staff of the Experimental Field number 6 of the Experimental Station at Balcarce for their excellent assis-
G.M. Rivera et al. / Animal Reproduction Science 36 (1994) I - I I
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tance. We also thank Drs. Alfredo Castro-Vazquez and Graciela A. Jahn of LARLAC-CRICYT for helpful criticism of the manuscript. References Adashi, E.Y., Resnick, C.E., Brodie, A.M., Svoboda, M.E. and Van Wyk, J.J., 1985. Somatomedin C mediated potentiation of follicle stimulating hormone induced aromatase activity of cultured rat granulosa cells. Endocrinology, 117:2313-2320. Alberio, R., Butler, H.M., Palma, G., Schiersmann, G.C.S., Algorta, D. and Ortiz, A., 1984. Actividad reproductiva y fertilidad luego de un destete temporario en vacas de cria multiparas con diferentes estados corporales. Rev. Arg. Prod. Anim., 4: 555-566. Baird, D.T., 1992. Luteotrophic control of the corpus luteum. Anim. Reprod. Sci., 28: 95-102. Bonavera, J.J., Verg6s, E. and Tortonese, D.J., 1987. Radioimmunoanalisisde progesterona en plasma bovino. Comparaci6n del uso del 125I y del 3H como trazadores. Acta Bioq. Clin. Latinoamericana, 21: 67-74. Bonavera, J.J., Schiersmann, G.C.S., Alberio, R.H. and Mestre, J., 1990. A note on the effects of 72hour calf removal and/or bull exposure upon post-partum reproductive performance. Anim. Prod., 50: 202-206. CaUejas, S.S., Alberio, R., Doray, J., Schiersmann, G. and Teruel, M., 1992. Caracteristicas de los ciclos estrales inducidos por el destete temporario, benzoato de estradiol y la combinaci6n de ambos en el postparto de vacas de cria. XIII Congreso Panamericano de Ciencias Veterinarias. Santiago, Chile. Abstract, p. 27. Carruthers, T.D., Convey, E.M., Kesner, J.S., Hafs, H.D. and Cheng, K.W., 1980. The hypothalamopituitary gonadotrophic axis of suckled and nonsuckled dairy cows postpartum. J. Anim. Sci., 51: 949-957. Convey, E.M., Tucker, H.A. and Short, R.E., 1983. Acute effect of suckling on gonadotropin, prolactin and glucocorticoid concentrations in serum of intact and ovarieetomised beef cows. Theriogenology, 20:661-674. Corah, L.R., Weel, A.P., Dunn, T.G. and Kaltenbach, C.C., 1974. Prepartum and postpartum levels of progesterone and estradiol in beef heifers fed two levels of energy. J. Anim. Sci., 39: 380-385. Cruz, C.L. and Kesler, D.J., 1988. Relationships of GnRH induced LH and FSH profiles on the ovulation responses and corpus luteum function of postpartum suckled cows. In: 1lth International Congress on Animal Reproduction and A.I. Dublin, Ireland. Vol l, p. 18. Driancourt, M.A., 199 I. Follicular dynamics in sheep and cattle. Theriogenology, 35: 55-79. Dunn, O.J., 1964. Multiple comparisons using rank sums. Technometrics, 6:241-252. Edwards, S., 1985. The effects of short term calf removal on pulsatile secretion in the postpartum beef cows. Theriogenology, 23: 777-785. Eger, S., Shemesh, M., Schindler, H., Amir, S. and Foote, R.H., 1988. Characterization of short luteal cycles in the early post-partum period and their relation to reproductive performance of dairy cows. Anim. Reprod. Sci., 16:215-224. Fernandes, L.C., Thatcher, W.W., Wilcox, C.J. and Call, E.P., 1978. LH release in response to GnRH during the postpartum period of dairy cows. J. Anim. Sci., 46: 443-448. Garverick, H.A., Zollers, W.G. and Smith, M.F., 1992. Mechanisms associated with corpus luteum lifespan in animals having normal or subnormal luteal function. Anim. Reprod. Sci., 28:11 l - 124. Gauthier, D., Blanc, M.R., Petit, M. and Pelletier, J., 1982. FSH and LH variation in beef cows during the postpartum period. Reprod. Nutr. Dev., 22: 283-290. Habich, G.E., Verde, L., Schiersmann, G.C.S. and Carrillo, J., 1974. Efecto de la restricci6n en el aporte energ6tico seguida de realimentaci6n sobre la reanudaci6n de los ciclos estrales de vacas Aberdeen Angus post-partum. Prod. Anim., 5:11 l-128. Hinshelwood, M.M., Dierschke, D.J. and Hauser, E.R., 1987. The effect of bovine follicular fluid on follicle-stimulating hormone (FSH) concentrations in beef cows in the early postpartum period. Biol. Reprod., 36: Suppl. 1,153. Humphrey, W.D., Kaltenbach, C.C., Dunn, T.G., Koritnik, D.R. and Niswender, G.D., 1983. Char-
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acterization of hormonal patterns in beef cows during the postpartum anestrus. J. Anim. Sci., 56: 445-453. INDEC, 1988. Censo Nacional Agropecuario. Ministerio de Economia. Buenos Aires, Argentina. Kaneko, H., Terada, T., Taya, K., Watanabe, G., Sasamoto, S. Hasegawa, Y. and Igarashi, M., 1991. Ovarian follicular dynamics and concentrations of oestradiol-17p, progesterone, luteinizing hormone and follicle stimulating hormone during the periovulatory phase of the oestrous cycle in the cow. Reprod. Fertil. Dev., 3: 529-535. King, G.J., 1984. Normal, short and long postpartum estrous cycles in dairy and beef cows. In: Proc. X Int. Cong. Animal Reproduction and A.I. Illinois, Vol. 3, pp. 399-401. Lamming, G.E., Wathes, D.C. and Peters, A.R., 1981. Endocrine patterns of the postpartum cows. J. Reprod. Fertil. Suppl. 30: 155-170. Leung, K., Padmanabhan, V., Spicer, L.J., Tucker, H.A., Short, R.E. and Convey, E.M., 1986. Relationship between pituitary GnRH-binding sites and pituitary release of gonadotrophins in postpartum beef cows. J. Reprod. Fertil., 76: 53-63. Lishman, A.W., Allison, R.L., Fogwell, R.L., Butcher, R.L. and Inskeep, E.K., 1979. Follicular development and function of induced corpora lutea in underfed postpartum anestrous beef cows. J. Anita. Sci., 48: 867-875. Lobb, D.K. and Dorrington, J., 1992. Intraovarian regulation of follicular development. Anita. Reprod. Sci., 28: 343-354. Manns, J.G., Humphrey, W.D., Flood, R.J., Mapletoft, R.J., Rawlings, N. and Cheng, K.W., 1983. Endocrine profiles and functional characteristics of corpora lutea following onset of postpartum ovarian activity in beef cows. Can. J. Anita. Sci., 63:331-347. McLeod, B.J. and McNeilly, A.S., 1987. Suppression of plasma FSH concentrations with bovine follicular fluid blocks ovulation in GnRH-treated seasonally anoestrous ewes. J. Reprod. Fertil., 81: 187-194. McLeod, B.J., Haresign, W. and Lamming, G.E., 1982a. The induction of ovulation and luteal function in seasonally anoestrous ewes treated with small-dose multiple injections of GnRH. J. Reprod. Fertil., 65:215-221. McLeod, B.J., Haresign, W. and Lamming, G.E., 1982b. Response of seasonally anoestrous ewes to small-dose multiple injections of GnRH with and without progesterone treatment. J. Reprod. Fertil., 65: 223-230. McNatty, K.P., Hudson, N., Gibb, M., Ball, K., Fannin, J., Kieboom, L. and Thurley, D.C., 1984. Effects of long-term treatment with LH on induction of cyclic ovarian activity in seasonally anoestrous ewes. J. Endocrinol., 100: 67-73. McNatty, K.P., Hudson, N., Gibb, M., Ball, K., Henderson, K.M., Heath, D.A., Lun, S. and Kieboom, L.E., 1985. FSH influences follicle viability, oestradiol biosynthesis and ovulation rate in Romney ewes. J. Reprod. Fertil., 75: 121-131. Odde, K.G., Ward, H.S., Kiracofe, G.H., Mc Kee, R.M. and Kittok, R.J., 1980. Short estrous cycles and associated serum progesterone levels in beef cows. Theriogenology, 14:105-112. Picton, H.M., Tsonis, C.G. and McNeilly, A.S., 1990. FSH causes a time-dependent stimulation of preovulatory follicle growth in the absence of pulsatile LH secretion in ewes chronically treated with gonadotrophin-releasing hormone. J. Endocrinol., 126: 297-307. Rawlings, N.C., Weir, L., Todd, B., Manns, J. and Hyland, J.H., 1980. Some endocrine changes associated with the postpartum period of the suckling beef cow. J. Reprod. Fertil., 60:301-308. Roche, J.F., Crowc, M.A. and Boland, M.P., 1992. Postpartum anoestrus in dairy and beef cows. Anita. Reprod. Sci., 28: 371-378. Schallenberger, E., Oerterer, U. and Hutterer, G., 1982. Neuroendocrine regulation of post-partum function. In: H. Karg and E. Schallenberger (Editors), Factors Influencing Fertility in the Postpartum Cow. Current Topics of Veterinary Medicine and Animal Science. Martinus Nijhoff, The Hague, Vol 20, pp. 123-147. Schams, D., Schallemberger, E., Menzer, Ch., Stangl, J., Zottmeir, K., Hoffman, B. and Karg, H., 1978. Profiles of LH, FSH and progesterone in post-partum dairy cows and their relation to the commencement of cyclic functions. Theriogenology, 10: 453-468. Sheffel, C.E., Pratt, B.R., Ferrel, W.L. and Inskeep, E.K., 1982. Induced corpora lutea in the postpar-
G.M. Rivera et al. / Animal Reproduction Science 36 (1994) 1-11
11
tum beef cow. II. Effects of treatment with progestogen and gonadotropins. J. Anim. Sci., 54: 830835. Shively, T.E. and Williams, G.L., 1989. Patterns of tonic luteinizing hormone release and ovulation frequency in suckled anestrous beef cows following varying intervals of temporary weaning. Domest. Anim. Endocrinol., 6: 379-387. Short, R.E., Bellows, R.H., Moody, E.L. and Howland, B.E., 1972. Effect of suckling and mastectomy on bovine postpartum reproduction. J. Anim. Sci., 34: 70-74. Short, R.E., Bellows, R.H., Staigmiller, R.B., Berardinelli, J.G. and Custer, E.E., 1990. Physiological mechanisms controlling anestrus and infertility in postpartum beef cattle. J. Anim. Sci., 68: 799816. Smith, M.F., Lishman, A.W., Lewis, G.S., Harms, P.G., Ellersieck, M.R., Inskeep, E.K., Wiltbank, J.N. and Amoss, M.S., 1983. Pituitary and ovarian responses to gonadotropin releasing hormone, calf removal and progestogen in anestrous beef cows. J. Anim. Sci., 57: 418-424. Snedecor, G.W. and Cochran, W.G., 1980. Statistical Methods. Iowa State University Press, Ames, IA. Waiters, D.L., Kaltenbach, C.C., Dunn, T.G. and Short, R.E., 1982a. Pituitary and ovarian function in postpartum beef cows. I. Effect of suckling on serum and follicular fluid hormones and follicular gonadotropin receptors. Biol. Reprod., 26: 640-646. Walters, D.L., Smith, M.F., Harms, P.G. and Wiltbank, J.N., 1982b. Effects of steroids and/or 48 hr calf removal on serum luteinizing hormone concentrations in anestrous beef cows. Theriogenology, 18: 349-355. Williams, G.L., 1990. Suckling as regulator of postpartum rebreeding in cattle: a review. J. Anim. Sci., 68: 831-852. Williams, G.L., Talavera, F., Petersen, J.B., Kirsch, J.D. and Tilton, J.E., 1983. Coincident secretion of follicle-stimulating hormone and luteinizinghormone in postpartum beef cows: effects of suckling and low level increases of systemic progesterone. Biol. Reprod., 29: 362-373. Williams, G.L., Koziorowski, M., Osborn, R.G., Kirsch, J.D. and Slanger, W.D., 1987. The postweaning rise of tonic luteinizinghormone secretion in anestrous cows is not prevented by chronic milking or the physical presence of the calf. Biol. Reprod., 36:1079-1084. Wright, I.A., Rhind, S.M., Russel, J.F., Whyte, T.K., McBean, A.J. and McMillen, S.R., 1987. Effects of body condition, food intake and temporary calf separation on the duration of the post-partum anoestrous period and associated LH, FSH and prolactin concentrations in beef cows. Anim. Prod., 45: 395-402.