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Introduction of bulls at different days postpartum on resumption of ovarian cycling activity in primiparous beef cows¹

Department of Animal and Range Sciences, Montana State University, Bozeman 59717

	Abstract

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The objective of this study was to evaluate postpartum resumption of ovulatory cycles among primiparous, suckled beef cows that were exposed continuously to mature bulls beginning at various intervals after calving. We sought to determine whether cumulative distributions of proportions of cows resuming ovarian cycles and interval from the start of bull exposure to resumption of ovarian cycling activity differed among cows exposed continuously (BE) or not exposed (NE) to bulls beginning on d 15, 35, or 55 after calving. Angus x Hereford cows (n = 56) were assigned randomly to one of six treatments in a 2 (exposure type) x 3 (day exposed postpartum) factorial arrangement. Blood samples were collected from each cow starting on d –1, and every third day until the end of experiment. An increase in baseline progesterone concentrations that exceeded 1.0 ng/mL in three consecutive samples was used as evidence of resumption of ovarian cycling activity. More (P < 0.05) BE cows resumed cycling activity by the end of the experiment than NE cows. Proportions of cows resuming cycling activity did not differ (P = 0.30) among cows exposed to bulls on d 15, 35, or 55 postpartum. Proportions of BE cows that were exposed to bulls on d 15, 35, or 55 were greater for each 10-d interval (P < 0.05) than those for NE cows during the first 40 d after exposure. More (P < 0.05) BE cows exposed to bulls on d 55 resumed cycling activity by 30 d after exposure than BE cows exposed to bulls on either d 15 or 35. Interval from calving to resumption of cycling activity was decreased (P < 0.05) by the presence of bulls. Day of exposure did not affect (P = 0.21) interval from calving to resumption of cycling activity; however, interval from day of bull exposure to resumption of cycling activity decreased (P < 0.05) linearly as day of exposure to bulls after calving increased. We conclude that exposing primiparous beef cows to bulls decreased the postpartum anovulatory interval and increased the proportion of cows that exhibit resumption of ovarian cycling activity, independent of day of bull exposure. Furthermore, cows exposed to bulls at progressively later intervals postpartum seemed to respond more rapidly to the biostimulatory effect of bulls than when they were exposed earlier in the postpartum anestrous period.

Key Words: Biostimulation • Bulls • Bovine • Cycling Activity • Postpartum Interval

	Introduction

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Exposing postpartum multiparous (Zalesky et al., 1984) and primiparous (Custer et al., 1990; Fernandez et al., 1993) suckled beef cows to bulls accelerates resumption of ovarian cycling activity. Factors that affect the response of postpartum anestrous cows to the biostimulatory effect of bulls are not well understood. Few studies have addressed the temporal development of this effect during postpartum anestrus in primiparous cows. Previous studies indicated that exposing primiparous suckled beef cows to bulls on d 30 after calving was as effective as exposing cows on d 3 after calving in decreasing the postpartum anestrous interval (Fernandez et al., 1993, 1996). Furthermore, there is indirect evidence that more multiparous cows resume ovarian cycling activity in a shorter period of time after bull exposure when they are exposed to bulls 50 or more days after calving than when they were exposed to bulls before 50 d after calving (Zalesky et al., 1984; Azzam et al., 1991). The temporal development of the response of postpartum anestrous cows to the biostimulatory effect of bulls is critical to understanding this effect and to designing experiments to discover the mechanism(s) whereby bulls affect postpartum reproductive activity of cows.

The question we wished to answer in the following study was whether primiparous suckled cows are more sensitive to the biostimulatory effect of bulls when exposure to bulls occurs at progressively longer intervals after calving. The objective was to evaluate the effect of bull exposure at longer intervals after calving on resumption of ovarian cycling activity in postpartum primiparous suckled beef cows. The null hypotheses tested in this experiment were that cumulative distributions of proportions of cows initiating ovarian cycles within 60 d after bull exposure and intervals to resumption of ovarian cycling activity from calving or from day of exposure to bulls do not differ among primiparous suckled cows not exposed or exposed continuously to mature bulls beginning on d 15, 35, or 55 postpartum.

	Materials and Methods

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Animals and Treatments
Fifty-six spring-calving, Angus x Hereford primiparous cows (24.1 ± 0.5 mo of age; mean ± SE), and six 2-yr-old, bilaterally epididectomized Angus x Hereford bulls were used in this experiment conducted at the Bozeman Livestock Teaching and Research Center at Montana State University. The calving season began January 22 and ended March 1, 2000. The experimental period extended from February 2 to May 23 (112 d). Body weight and BCS (Richards et al., 1986) were obtained within 3 d after calving and were 495 ± 74 kg and 4.7 ± 0.6, respectively.

Bulls underwent a standard libido test 3 wk before the start of the calving season (Chenoweth, 1983). Cows were stratified by calving date, dystocia score, calf BW, and sex of calf within 3 d of calving and assigned randomly to one of six treatments in a completely randomized design using a 2 x 3 factorial arrangement. Factors were exposure type (bull or no bull exposure) and day exposed postpartum (15, 35, or 55). Day 15, 35, or 55 postpartum represented d 0 for each treatment, respectively. All experimental procedures and animal-handling and care protocols used in this experiment were approved by the Montana State University Institutional Animal Care and Use Committee.

Lots Used for Exposure Type
Two lots were used for this experiment, designated north and south by their geographic location. Each lot contained four 41 x 18 m (length x width) pens that were identical in east-west configuration, bunk space, aspect, slope, and connection to open-shed shelters. Lots were approximately 0.35 km apart, and the arrangement was such that the prevailing wind blew from the south to the north. Animals housed in one lot were not able to see or smell animals housed in the other lot; however, there was a possibility that sounds made by animals in one area could be heard by animals in the other area. These lots and arrangement have proven to be effective in previous experiments involving bull-cow interactions (Fernandez et al., 1993; 1996). Bulls had not been housed in these pens for the previous 3 yr.

Bull Exposure
Pens within the north lot were used for maintaining cows in treatments that included bulls (BE), whereas pens within the south lot were used for maintaining cows in treatments that did not include exposure to bulls (NE). Cows assigned to either BE or NE treatments were placed into pens on d 0. Cows assigned to the BE treatments were placed in a pen, chosen randomly, containing one bull in the north lot for each treatment. The bull-to-cow ratio for each pen was approximately 1:9. Likewise, cows assigned to the NE treatments were placed in a clean pen, chosen randomly, in the south lot. Pens in each lot were isolated from each other by draping and securing tarpaulins over the 3-m fences that separated pens. Cows exposed to bulls had no contact with bulls throughout pregnancy and after calving until they were placed in pens with bulls on d 15, 35, or 55 postpartum. Cows not exposed to bulls had no contact with bulls throughout pregnancy and the experiment.

Nutrition
Cows and calves had free access to good-quality mixed-grass alfalfa hay and any pasture grasses that were available before they were moved into their respective pens. Once cows were moved into pens, they were given free access to the same hay (chopped), 0.25 kg of cracked barley per animal daily (as-fed basis), water, and a mineralized-salt supplement (Cargill, Minneapolis, MN) until the end of the experiment. The TDN of the diet exceeded the NRC (1996) requirement for lactating beef cows with a mature weight of 545 kg by approximately 18%. Bulls were fed the same diet as cows.

Blood Sampling and Progesterone Assay
Blood samples (7 mL) were obtained from each cow in each treatment by jugular venipuncture starting 1 d before d 15, 35, or 55 postpartum, and every third day from the time of exposure until the end of the experiment (May 23). Samples were placed on ice, allowed to clot overnight at 4°C, and centrifuged at 1,850 x g for 30 min at 4°C.

Serum was harvested and stored at –20°C until assayed for progesterone. Progesterone was assayed using solid-phase RIA kits (Diagnostic Products Corp., Los Angeles, CA) validated in our laboratory for bovine serum (Custer et al., 1990). The sensitivity of this assay was 0.03 ng/mL. Intra- and interassay CV for a serum pool that contained 0.42 ng/mL were 6.2 and 12.3%, respectively; and for a pool that contained 3.1 ng/mL were 2.6 and 6.9%, respectively. Changes in progesterone concentrations were used to assess the resumption of ovarian cycling activity. An increase in baseline progesterone concentrations in three consecutive samples that exceeded 1.0 ng/mL during the experimental period was used as the criterion for resumption of ovarian cycling activity. The graphic representation of the pattern of progesterone concentrations used to validate this criterion is given in Fernandez et al. (1993) for primiparous suckled beef cows.

Statistical Analyses
Postpartum resumption of ovarian cycling activity for cows that had not exhibited an increase in progesterone by the end of the experiment was calculated by assuming that resumption of cycling activity occurred 7 d after the end of the experiment, then subtracting calving date from this day for all cows or d 0 for cows exposed to bulls.

Proportions of cows among treatments that exhibited resumption of ovarian cycling activity by the end of the experiment were analyzed by contingency ² tests (Steel and Torrie, 1980). Cumulative percentage distributions for proportions of cows that resumed cycling activity were constructed for 10-d intervals after d 0. Proportions of cows among treatments that exhibited resumption of ovarian cycling activity for each 10-d interval were analyzed by contingency ² analyses (Steel and Torrie, 1980).

Data for postpartum interval to resumption of ovarian cycling activity from calving was analyzed by ANOVA for a completely randomized design with a factorial arrangement of treatments using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC). The model included exposure type (NE or BE), day exposed postpartum (15, 35, or 55), and the interaction between exposure type and day exposed postpartum. If interactions were not significant, main effect means were evaluated with Bonferroni’s t-test option of SAS. Intervals from bull exposure to resumption of ovarian cycling activity for cows exposed to bulls on d 15, 35, or 55 were analyzed by a one-way ANOVA. Means were separated using Bonferroni’s t-test option of SAS. Intervals were then evaluated by regression analysis using the REGRESS procedure of SAS.

	Results

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The proportion of cows that resumed ovarian cycles by the end of the experimental period was greater (P < 0.05) for BE cows (82%) than for NE cows (28%). In contrast, proportions of cows that resumed cycling activity did not differ (P = 0.30) among cows that were assigned to treatments on d 15, 35, or 55 postpartum, averaging 55%.

The cumulative distribution for proportions of cows resuming cycling activity at 10-d intervals after treatment is presented in Table 1. More (P < 0.05) cows exposed to bulls on d 55 resumed cycling activity by 20 and 30 d after exposure than cows exposed to bulls on either d 15 or 35 (Table 1). However, proportions of cows exposed to bulls on d 15, 35, or 55 that resumed cycling activity by 40, 50, and 60 d did not differ but were greater (P < 0.05) than those for cows not exposed to bulls over these intervals (Table 1).

	Discussion

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The design of the present study allowed us to evaluate the nature of how cows respond to the biostimulatory effect of bulls when exposed at different times during the postpartum anestrous period. Examination of the cumulative proportions of cows resuming cycling activity at 10-d intervals after bull exposure on d 15, 35, or 55 indicated that the biostimulatory effect of bulls manifested itself within the first 20 to 30 d if exposure began on d 55 after calving. Cows exposed to bulls on d 15 or 35 after calving required significantly more exposure time (between 30 to 40 d or longer) to exhibit the same percentage of response as cows exposed to bulls on d 55 after calving. These results indicate that cows exposed to bulls later in postpartum anestrus respond more rapidly to the biostimulatory effect of bulls than when exposure occurs early after calving. Evaluation of postpartum intervals from calving and from day of exposure to resumption of cycling activity supports this concept.

Inspection of the main effects of treatments indicated that interval from calving to resumption of cycling activity was decreased by bull exposure but not influenced by day after calving that cows were exposed to bulls. Nonetheless, the interaction between exposure type and day exposed to bulls after calving for interval from bull exposure to resumption of cycling activity indicated that cows were differentially affected by the day postpartum that cows were exposed to bulls. The interval from bull exposure to resumption of cycling activity decreased in a linear manner as day of exposure after calving increased. One interpretation of this result could be that primiparous cows become progressively more sensitive to the biostimulatory effect of bulls as time after calving increases. Another explanation for these results could be related to the effect of day of the calving season when cows calve. Bellows and Short (1978) and Smeaton et al. (1986) reported that beef cows that calved early in a spring calving season had shorter postpartum intervals to estrus than cows calving later in the spring. However, in our study, cows in each treatment were stratified by day of calving, precluding the probability that cows in any one treatment would be cows that calved late in the calving season. In fact, analysis of calving date indicated that calving date did not differ among treatments.

Present data and those of Custer et al. (1990) and Fernandez et al. (1993, 1996), who exposed primiparous suckled beef cows to bulls on d 3 (Custer et al., 1990) or 30 (Fernandez et al., 1993, 1996), indicate that exposing primiparous suckled beef cows to bulls on either d 3, 15, 30, 35, or 55 are equally effective in decreasing postpartum anovulation and increasing the proportions of cows resuming cycling activity before the beginning of the breeding season. Therefore, the biostimulatory effect of bulls seems to operate independently from day of exposure after calving if cows were exposed continuously to bulls.

Nonetheless, the aforementioned conclusion is not entirely accurate based on our results, and it requires further qualification and refinement. Perhaps the most important findings of this experiment are related to the cumulative distributions of percentages of cows cycling at 10-d intervals after exposing cows to bulls on d 15, 35, or 55, and intervals from bull exposure to resumption of cycling activity for cows within these treatments. Examination of these distributions and intervals indicated that the biostimulatory effect of bulls manifested itself more rapidly when cows were exposed to bulls on d 55 after calving than when cows were exposed to bulls on either 15 or 35 d after calving, and linearly decreased intervals from bull exposure to resumption of cycling activity as day of exposure increased. In support of these data, Fernandez et al. (1993) found that intervals from calving to resumption of cycling activity did not differ among cows exposed to bulls 3 d after calving, exposed to bulls on d 30 after calving, or cows exposed to bulls from d 3 to 30 only after calving. A closer inspection of the Fernandez et al. (1993) data revealed that the interval from bull exposure to resumption of cycling activity in cows exposed to bulls beginning on d 30 after calving was shorter than that for cows exposed to bulls from d 3 after calving. Zalesky et al. (1984) reported that a greater proportion of multiparous cows exhibited estrus by d 53 after calving when bulls were introduced to cows on d 3 after calving than when bulls were introduced to cows on d 53 postpartum. However, we reexamined the data from that study relative to the rate of change in proportions of cows that showed estrus after exposure to bulls from either d 3 or 53 after calving. We found that the proportions of cows that resumed ovarian cycling at 10-d intervals after exposure to bulls on d 53 after calving was greater than those for cows exposed on d 3 after calving. Furthermore, data reported by Scott and Montgomery (1987) indicated that a similar rate of increase in cycling activity occurred in cows that were not exposed to bulls before 56 d after calving and then combined with bulls and cows that were exposed to bulls soon after calving. Therefore, exposing cows to bulls after 30 d or later after calving seems to accelerate the increase in the proportions of cows that respond to the biostimulatory effect of bulls.

The mechanism whereby bulls accelerate resumption of ovarian cycling activity in postpartum suckled beef cows is unknown. Ultimately, the biostimulatory effect of bulls alters secretory pattern of LH that culminate in ovulation (Custer et al., 1990; Fernandez et al., 1996). For this to occur, the biostimulatory effect of bulls must in some way modify the GnRH neuronal system in a manner that is analogous to but opposite in nature, to that involved with the establishment of the cow-calf bond (Williams et al., 1995). The biostimulatory effect of bulls may be mediated directly or indirectly by 1) attenuation of the negative feedback effect of estradiol-17ß on the tonic release of the hypothalamic mechanisms regulating GnRH release; 2) attenuation of the negative feedback effects associated with maternal bonding and suckling; 3) a reduction in hypothalamic opioid tone; 4) by a direct effect that stimulates hypothalamic mechanisms controlling GnRH release; or 5) through combinations of these physiological mechanisms. Whatever the exact mechanism(s), the biostimulatory effect of bulls seems to involve a temporal evolution of interacting mechanisms among the sensory, neuroendocrine, and reproductive endocrine systems of the postpartum anestrous cow that result in an accelerated resumption of ovarian cycling activity.

In conclusion, primiparous suckled beef cows are more likely to respond sooner to the biostimulatory effect of bulls if they are exposed to bulls at progressively longer times after calving. The biostimulatory effect of bulls seems to operate through the same underlying sensory-neuroendocrine-endocrine mechanism(s) independent of time after calving, if the time after calving is greater than 15 d. However, responsiveness of this mechanism to the presence of bulls seems to be more rapid after d 35 than before d 35, presumably due to a decrease in negative feedback to estradiol, attenuation of the cow-calf bonding, decrease of suckling stimuli, or some other neuroendocrine-endocrine pathway. These findings may be beneficial for further investigations into the mechanism of the biostimulatory effect of bulls, and for developing reproductive management strategies that include bulls to increase reproductive efficiency of postpartum primiparous suckled beef cows.

	Footnotes

 
¹ This study was supported by National Research Initiative Grant 99-35203-7932 from the USDA Cooperative State Research, Education, and Extension Service and the Montana Agric. Exp. Stn. The authors express their gratitude to R. Adair, M. McKamey, T. Spinner, S. Berardinelli, K. Berardinelli, B. Robinson, and K. Anderson for their dedication and excellent technical assistance during the course of this study.

³ Current address: The Ohio State University, 185 Hamilton, 1645 Neil Ave., Columbus 43210.

² Correspondence—phone: 406-994-5574; fax: 406-994-5589; e-mail: jgb{at}montana.edu.

Received for publication December 29, 2004. Accepted for publication May 3, 2005.

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